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date: 17 August 2018

Visual Development

Summary and Keywords

Human visual development is a complex dynamic psychological/neurobiological process, being part of the developing systems for cognition, action, and attention. This article reviews current knowledge and methods of study of human visual development in infancy and childhood, in relation to typical early visual brain development, and how it can change in developmental disorders, both acquired (e.g., related to at-risk births) and genetic disorders. The newborn infant starts life with a functioning subcortical visual system which controls newborn orienting to nearby high contrast objects and faces. Although visual cortex may be active from birth, its characteristic stimulus selectivity and control of visual responses is generally seen to emerge around six to twelve weeks after birth. By age six months the infant has adequate acuity and contrast sensitivity in nearby space, and operating cortical mechanisms for discriminating colors, shapes, faces, movement, stereo depth, and distance of objects, as well as the ability to focus and shift attention between objects of interest. This may include both feedforward and feedback pathways between cortical areas and between cortical and subcortical areas. Two cortical streams start to develop and become interlinked, the dorsal stream underpinning motion, spatial perception and actions, and the ventral stream for recognition of objects and faces. The neural systems developing control and planning of actions include those for directed eye movements, reaching and grasping, and the beginnings of locomotion, with these action systems being integrated into the other developing subcortical and cortical visual networks by one year of age. Analysis of global static form (pattern) and global motion processing allows the development of dorsal and ventral streams to be monitored from infancy through childhood. The development of attention, visuomotor control and spatial cognition in the first years show aspects of function related to the developing dorsal stream, and their integration with the ventral stream.

The milestones of typical visual development can be used to characterize visual and visuo-cognitive disorders early in life, such as in infants with perinatal brain injuries and those born very prematurely. The concept of “dorsal stream vulnerability” is outlined. It was initially based on deficits in global motion sensitivity relative to static form sensitivity, but can be extended to the planning and execution of visuomotor actions and problems of attention, together with visuospatial and numerical cognition. These problems are found in the phenotype of children with both genetic developmental disorders (e.g., Williams syndrome, autism, fragile-X, and dyslexia), and in acquired developmental disorders related to very preterm birth, or in children with abnormal visual input such as congenital cataract, refractive errors, or amblyopia. However, there are subtle differences in the manifestation of these disorders which may also vary considerably across individuals. Development in these clinical conditions illustrates the early, but limited, plasticity of visual brain mechanisms, and provides a challenge for the future in designing successful intervention and treatment.

Keywords: visual development, brain development, infancy, visual disorders, dorsal stream vulnerability

Key Points

  1. 1. Visual development cannot be separated from the dynamic processes of development of cognition, attention, and the control of actions.

  2. 2. The typically developing infant shows visual responses from birth which are initially largely controlled by subcortical eye-brain networks.

  3. 3. During the first few months of life the visual cortex starts to take over control of subcortical networks to control visual behavior. There is development of both feedforward and feedback mechanisms, continuing from infancy throughout childhood into adulthood.

  4. 4. Improvement in visual acuity (fineness of vision) results from a combination of development of the retinal photoreceptors, and maturation of neural systems, provided the visual input to the eyes is normal. Adult levels of acuity are reached by around six to seven years of age.

  5. 5. A complex sequence of functional development in cortical modules in the first six months of life underpins the infant’s sensitivity to contour orientation, directional motion, color, and depth.

  6. 6. This development of the cortex includes development of binocular interaction and development of the two main cortical streams, the dorsal stream—underpinning global motion processing and visual control of actions, and the ventral stream—underpinning global form and pattern processing, and recognition of objects and faces. In everyday vision, processing in ventral and dorsal streams is interlinked.

  7. 7. Distinct action systems for controlling eye movements, manual actions, and locomotion start to function in the first year of life, but are not mature for many years later.

  8. 8. Development of attentional neural systems is linked to networks within the dorsal and ventral streams in the first years of life.

  9. 9. There is a progressive improvement in accommodation and reduction of refractive error (“emmetropization”) in infancy, including the reduction of astigmatism. Infants with hyperopic refractive errors are at risk of strabismus and amblyopia, risks which can be reduced by early spectacle correction.

  10. 10. The effects of early visual deprivation (amblyopia) and recovery indicate the high plasticity of visual brain networks in an early critical period. However, some plasticity is maintained even in the adult visual brain.

  11. 11. The development of visual brain networks is a factor in many developmental disorders. “Dorsal stream vulnerability” is a cluster of deficits or delays in processing by the dorsal compared to the ventral stream, which affects global motion sensitivity relative to static form coherence, visuomotor and spatial cognition, visual attention, and numerical ability. This cluster of problems is common to many neurodevelopmental disorders, both genetic and acquired. These functions show individual variations in typically developing children, associated with the structure of the parietal lobe and its connectivity. Delays or deficits in dorsal stream processing may have knock-on effects for integration needed for everyday vision across ventral and dorsal streams.

  12. 12. This dorsal stream network may overlap with a developing “multiple demand” system, which has been identified in the adult brain.

  13. 13. New tests are being developed which are child-friendly and age-appropriate for typically developing infants and children, and those with developmental disorders. These tests make possible identification, diagnosis, and treatment of visual disorders early in life.


Visual development is a key area for early child development, for several reasons. First, vision is the main sensory channel for information about objects and space beyond our body surface, and also a major channel for information about other people and their actions. Visual capabilities develop rapidly in infancy, underpinning the child’s developing understanding of the physical and social world.

Secondly, psychology, medicine, and neuroscience have provided a deeper understanding of vision than for any other area of cognitive processing, including a rich knowledge of the eye and brain mechanisms underlying visual function. This includes the early development of these mechanisms in other species, which can provide a valuable model for human development. Thus, vision is in the vanguard for the new science of developmental cognitive neuroscience, linking neural development to emerging capabilities in vision and visual cognition.

Thirdly, the early development of vision in infancy, and the available techniques for investigating it, mean that vision provides a window into the developing brain more generally. In investigating early developmental disorders (e.g., perinatal brain damage), visual assessment offers a possible early surrogate outcome measure for later motor, cognitive and social development.

Psychologists commonly distinguish “perception” “cognition” and “action” However, both in development and adulthood, these processes involve an interconnected network of brain systems. Directing attention, recognizing objects, and acting towards the position of objects in space, are interlocked closely in development and it is not helpful to consider vision in isolation from the ways it contributes to the child’s achievement of behavioral goals. This article takes a broadly neurobiological approach, which considers vision as part of a dynamic, integrated, developing neural system, focusing on the striking changes in visual abilities and the parallel changes in eye-brain function and structure in the first years of life.

Recent work has highlighted how far visual development continues through childhood and adolescence, and can even be plastic in adulthood, but a full discussion of this is beyond the scope of this article.

Outline of Visual Processing

To understand visual development, an outline of the structure and function of the visual system will be helpful. Technical terms which are explained in the glossary are given in italics at their first appearance.

An optical image of the visual world is formed on the retina of each eye, and encoded into neural signals by photoreceptor cells (rods and cones) which are progressively transformed, through the neural network of the retina and via the optic nerves to a series of interconnected brain areas. This pathway includes the LGN (lateral geniculate nucleus), a nucleus of the thalamus, where the fibers of the optic nerve terminate and which is the major relay station of sensory information on the way to the cortex.

The striate cortex (area V1), in the occipital lobe of the brain, contains neurons which are specialized to extract various kinds of information, notably the orientation of lines and edges, directions of motion, and to bring together information from the two eyes for depth perception based on binocular disparity (stereopsis). This is generally called local visual processing. A series of extrastriate visual areas, such as V2, V3, V4, and V5, have distinct specializations of function; for example V5 or MT (Zeki, 1974) combines directional information coming from V1 to detect global patterns of motion over larger spatial areas than in V1. Another example is LO (lateral occipital), an area specialized for the structure of objects and scenes, and the PPA (parahippocampal place area), found to be part of the network for recognizing scenes and navigation. Pathways through these extrastriate areas send information to the temporal and parietal lobes of the brain forming two functionally distinct information-processing streams in the brain. The ventral stream, passing to the temporal lobe, is specialized for recognizing shapes and objects, including human faces, while the dorsal stream, passing to the parietal lobe (including the PPC—posterior parietal complex) encodes the spatial and motion information needed for visually guided actions. The components of the dorsal stream, and their roles in action control, attention, and spatial cognition, are described more fully in later sections.

A minority of fibers in the optic nerve do not connect to the cerebral cortex, but to midbrain structures, particularly the superior colliculus. The colliculus serves to control eye movements, in particular saccades, the abrupt movements which shift gaze from one object to another. Midbrain nuclei also control smooth eye movements for following moving objects, and the reflex optokinetic nystagmus (OKN) which stabilizes vision when the whole field of view moves. In adults, all these eye movement functions interact strongly with the more complex analysis in the cortex, via connections between subcortical visual centers and visual cortical areas.

A further set of pathways involves the pulvinar nucleus of the thalamus, which is increasingly viewed as a key structure for information transmission to and from the cortex (Shipp, 2003, 2004). Recently, neural connections from MT in extrastriate cortex, bypassing V1, have been found in marmosets (Warner, Kwan, & Bourne, 2012) and in adult humans whose V1 route has been damaged (Barbur, Watson, Frackowiak, & Zeki, 1993; Ajina & Bridge, 2016). This pathway has been called the “lateral pathway” (Gilaie-Dotan, 2016). These direct links, partly via the pulvinar, have been thought to be important as the neural underpinnings of certain types of motion processing and visual attention. Another pathway from subcortical structures to areas processing face-like configurations may also be involved in face recognition (Johnson, Senju, & Tomalski, 2015). However, to date we have very little evidence about the role of these additional pathways and how they develop in human infancy and childhood.

Neurobiological Model of Visual Development

Visual DevelopmentClick to view larger

Figure 1. Model of the Development of Visual Brain Systems, and the Behavior they Control, on the Timeline (left) from Birth to One Year of Age, Updated from Atkinson (2000) and Atkinson and Braddick (2012b). The early connections through the pulvinar shown in orange have been suggested (e.g., Johnson et al., 2015; Warner et al., 2012), although such links have not been demonstrated in human development.

Figure 1 schematically presents a neurobiological model of early visual development emphasizing feedforward processes, although feedback mechanisms are undoubtedly important (and at present less well understood, developmentally). This model was first put forward for typical visual development in the first year of life by Atkinson (1984, 2000; Atkinson & Braddick, 2003), with recently suggested extensions (Atkinson, 2017). Its main features are:

  • primarily subcortical visual function at birth, with a rapid postnatal onset of cortical visual systems, including feedback systems;

  • progression from local (striate) to global (extrastriate) cortical functioning;

  • distinct developmental courses for dorsal and ventral cortical streams; and

  • dorsal stream linked to visually controlled action modules and to the modulation of these by attention processes.

Subcortical and Cortical Visual Systems

Studies in rodents in the 1960s showed that cortical damage impaired pattern discrimination (a “what” response), while subcortical damage to the superior colliculus impaired orienting responses to significant stimuli (a “where” response; Sprague & Meikle, 1965; Schneider, 1969). Newborn human infants can orient by head and eye movements to conspicuous visual and auditory stimuli in the near periphery, but show little evidence of pattern discrimination, suggesting that subcortical vision at birth can locate where a stimulus event is, but postnatal maturation of the visual cortex is required to identify “what” is there (Bronson, 1974). It is not yet known how far the newborn’s cortical mechanisms are inactive, and how far they are active but too noisy or poorly organized to be effectively functional.

However, in the first days of life newborn infants are able to make a discriminatory response to a face-like configuration of three high contrast blobs (e.g., Goren, Sarty, & Wu, 1975; Johnson, Dziurawiec, Ellis, & Morton, 1991; Johnson & Morton, 1991; Simion, Valenza, & Umilta, 1998; Simion, Di Giorgio, Leo, & Bardi, 2011) and to a familiar face compared to an unfamiliar face (e.g., face of mother versus other female face with same face coloring; Bushnell, Sai, & Mullin, 1989). In the latter case the infant uses the external contour of the hairline for recognition (an example of the “externality effect”; Milewski, 1976; Bushnell, 1982). A subcortical pathway, from superior colliculus to pulvinar, has been hypothesized as underpinning detection of this face-like configuration of three blobs, although there is still some debate about this (discussed in the section on face perception later in this article).

Evidence both from behavioral discrimination and from electroencephalogram (EEG) demonstrates the postnatal development of specific cortical functions, including populations of neurons underpinning orientation selectivity (for shape recognition), motion processing, binocularity, and some aspects of color and pattern vision, which all emerge between age one and six months (Atkinson, 1984; Braddick, Atkinson, & Wattam-Bell, 1989; Atkinson, 2000; Atkinson & Braddick, 2003). As detailed in later sections, these cortical functions do not emerge together but in an ordered sequence: orientation around the first few weeks of life, followed by directional motion selectivity (at five to nine weeks of age), and then binocular interaction for stereoscopic vision (two and a half to five months of age).

The cortical system does not simply replace the newborn’s subcortical vision system, but instead comes to modulate and control subcortical processing. This is evidenced by changes in the optokinetic response (eyes following a large moving field) and in the ability to disengage fixation from one target and transfer gaze to another. In both cases, newborn patterns of visual behavior persist in infants whose cortical processing is disrupted by surgical removal of one hemisphere (Braddick et al., 1992).

Dorsal and Ventral Streams

The model illustrated in Figure 1 includes the broad division in visual processing between the dorsal and ventral cortical streams. Among the cortical functions emerging in the early months, directionality and some aspects of stereopsis are associated with the dorsal stream network. The later emergence of these processes, compared to orientation and color selectivity, may indicate a relatively slower initial development of the dorsal pathways compared to the ventral stream. However, dorsal- and ventral-based functions have their distinctive developmental courses beyond this initial emergence, which is reviewed below. In everyday vision, information processed in both streams must be combined, for example for locating an identified object (Milner, 2017). Thus, delays in visual development may result from failure to combine dorsal and ventral stream information, as well as from deficits or delays in development within one or other stream.

Ventral and dorsal cortical streams have been distinguished not only by the types of visual information they process, but by their different behavioral functions—perception and recognition for the ventral stream, and visual control of action for the dorsal stream (Milner & Goodale, 1995, 2008). However, these distinctive functions of the dorsal and ventral streams should not be considered as absolute in everyday vision because of the complexity of feedforward and feedback neural networks within both streams, and the integration of information processing across streams and with subcortical areas. These two broad streams include multiple loosely connected modules; in particular, distinct dorsal stream visuomotor modules processing the information required for different action systems (orienting head and eyes, reaching, grasping, locomotion, etc.) The model of Figure 1 suggests that the emergence of these forms of behavior during the first year of life is associated with the establishment of distinct visuomotor modules (Atkinson & Braddick, 2003).

Many of the areas of the dorsal cortical stream are also those which have been implicated as elements of attentional systems in the adult human brain. As indicated in Figure 1, attention has a key role in selecting the targets for action and so modulating the activity of visuomotor modules. The development of attentional control is an important aspect of visual development, discussed in detail below.

Methods for Measuring Visual Development

Preferential Looking

Progress in understanding infants’ visual development, especially in early infancy, has rested on a specific armory of techniques (see Atkinson & Braddick, 1999) geared to the milestones indicated in Figure 1. Since eye and head movements are the best organized aspect of behavior in infants under six months, preferential looking has been a key method in this age range: if infants show a statistically reliable preference for fixating pattern A over pattern B (with both patterns visible together, side by side), this demonstrates that the infant is capable of visually discriminating the patterns (Fantz, 1961, 1964). For example, infants’ preference for a patterned over a blank field of the same average luminance, has been used as an indicator of the limits of infants’ acuity and contrast sensitivity (see the next section). Davida Teller realized that the most sensitive information about preference could be gained by the judgments of a “blind” observer who watched infants’ looking behavior while unaware of the relative positions of patterns A and B. This is called Forced Choice Preferential Looking or FPL. It was first used to measure acuity and contrast sensitivity in young infants (Atkinson, Braddick, & Braddick, 1974; Teller, Morse, Borton, & Regal, 1974), and exploited in the Teller Cards (McDonald et al., 1985), which have been used extensively in clinical settings over many years. New developments use automated eye tracking and multiple alternative stimulus locations (Jones, Kalwarowsky, Atkinson, Braddick, & Nardini, 2014; Jones, Kalwarowsky, Braddick, Atkinson, & Nardini, 2015.


Preferential looking depends on the infant having an intrinsic preference between the stimuli, but infants may be able to discriminate stimuli without preferring to look at one rather than the other. Habituation-recovery methods overcome this by exploiting a general preference for novelty. Infants’ looking time decreases (habituation) when repeatedly viewing a particular stimulus; a novel stimulus is then introduced, and if it is fixated for a significantly longer time than the habituated stimulus, then the infant must be sensitive to the difference between the two (Fantz, 1964). If the infant is habituated to a stimulus which is constant in one respect (e.g., physical shape) but variable in another (e.g., viewing angle), then looking time when the formerly constant property is changed (e.g., a new physical shape) can assess the infant’s ability for perceptual generalization (Caron, Caron, & Carlson, 1979). Habituation has been used extensively for gauging many different visual discriminations, for example geometrical shapes and faces, and to study color and form constancy. It also provides an approach to the measurement of visual attention.

Visual Event-Related Potentials

Behavioral measurements can be complemented by EEG measures called the visual evoked potential (VEP) or visual event-related potential (VERP). This is a visual response within the EEG, mass electrical neural activity recorded non-invasively from the surface of the infant’s head, which can be identified as a visual response because it is time-locked to a specified visual event. The method has the advantage that it does not require any controlled motor or verbal response from the participant, although it does require the infant to attend to the stimulus and to remain relatively still during recording. The signals are faint relative to background “noise,” so they have to be extracted by digital signal averaging. At slow presentation rates (transient VEP) a complex waveform with different components can be extracted. However there are advantages to the “steady state method” which generates a rhythmic electrical response for stimuli presented at rates of four per second and above (e.g., Harris, Atkinson, & Braddick, 1976; Atkinson & Braddick, 1999; Norcia, Appelbaum, Ales, Cottereau, & Rossion, 2015). A variant of steady state VEP is the sweep VEP, which has been used to measure visual acuity by identifying the highest spatial frequency to elicit a signal significantly above noise (Norcia & Tyler, 1985).

VEP/VERP responses can be obtained from different types of visual event: Table 1 lists VEP/VERP measures that tap increasingly complex processes. This approach has enabled researchers to identify the developmental sequence of these processes as summarized in the right-hand column. It should be noted that for the more complex types of processing (e.g., rows 3–5 in Table 1) careful design of stimulus sequences and analysis is required to isolate high-level processes from responses to simpler events, such as the local contrast changes that accompany complex pattern transitions. This can be done by separating different frequencies in the steady state response (“frequency tagging”) reflecting the high-level and low-level stimulus transitions (e.g., Atkinson & Braddick, 1999; Norcia et al., 2015; de Heering & Rossion, 2015).

Table 1. VEP Methods Probing Different Levels of the Developing Visual System



Appropriate Age


Light response—subcortical


From preterm

Shepherd, Saunders, McCulloch, and Dutton (1999)

Spatial contrast response—input to cortex—not necessarily Cortical processing

Pattern reversal—checkerboard (Phase reversal of grating pattern)

From term

Harris et al. (1976); McCulloch, Orbach, and Skarf (1999); Atkinson and Braddick (2013)

Developing selectivity of primary visual cortex

Orientation-reversal VERP

Eight weeks upwards

Braddick, Wattam-Bell, and Atkinson (1986); Braddick (1993); Mercuri et al. (1998, 1999); Atkinson et al. (2002c); Atkinson and Braddick (2008)

Direction-reversal VERP

Twelve weeks upwards

Wattam-Bell (1991); Braddick, Birtles, Wattam-Bell, and Atkinson (2005)

Binocular correlogram VERP

Twelve weeks upwards

Braddick et al. (1980); Braddick, Wattam-Bell, Day, and Atkinson (1983); Wattam-Bell, Braddick, Atkinson, and Day (1987); Smith, Atkinson, Anker, and Moore (1991)

Timing of cortical processing

“Calculated latency” of pattern reversal VERP

Birth onwards

Lee, Birtles, Wattam-Bell, Atkinson, and Braddick (2012)

Extrastriate global processing of motion (areas V5, V3a) and form (area V4)

Global motion- and form-coherence VERP

Three months onwards

Wattam-Bell et al. (2010); Braddick, Atkinson, and Wattam-Bell (2011)

Both behavioral and VERP measures require indirect inferences and assumptions to reach conclusions about functional vision (Atkinson & Braddick, 2013). Since these inferences are different, the most secure approach to infant vision is to make converging measurements of the same function using the two approaches. There are very few studies that have compared behavioral and VEP/VERP responses using matched stimuli, but one such developmental study on a single infant showed that very similar values of acuity and contrast sensitivity development were obtained across different techniques in the first months of life (Atkinson & Braddick, 1989; Atkinson, 2000).

High-density sensor arrays allow VERP signals to be mapped over the surface of the scalp, distinguishing signals arising from different anatomical sources in the brain. This can indicate the presence of distinct brain mechanisms, but the “inverse problem” of locating such sources has many uncertainties, especially in the infant brain (e.g., Reynolds & Richards, 2009).

Brain Imaging Techniques: MRI and NIRS

Adult cognitive neuroscience has been revolutionized by Magnetic Resonance Imaging (MRI) technologies, which allow detailed analysis of brain structure and connectivity, and identification of the pattern across and within brain areas of oxygenated blood flow associated with activity (functional MRI or fMRI). These methods depend on the participant remaining stationary within a few millimeters inside the magnetic scanner, so they are difficult to use with a young child who is conscious. However, an increasing number of developmental studies using MRI are being published, showing both the structural growth of visual and other areas (see Brown & Jernigan, 2012, for an overview) and the approach to maturity of functional patterns of activation during infancy and childhood (examples are Born et al., 2000; Conner, Sharma, Lemieux, & Mendola, 2004; Klaver et al., 2008; Dekker, Mareschal, Sereno, & Johnson, 2011; Dekker et al., 2015; Biagi, Crespi, Tosetti, & Morrone, 2015; Deen et al., 2017).

A less demanding, but spatially less precise method, tests brain activity through oxygenated blood flow measured by Near Infra Red Spectroscopy (NIRS), a method reviewed by Gervain et al. (2011). Localized activity in visual cortex was measured in this way in three-month-old infants by Meek et al. (1998), and infants’ brain activation by specific classes of stimuli has been explored, for example by Otsuka et al. (2007) and by Yang, Kanazawa, Yamaguchi, and Kuriki (2016). Technical refinements in both MRI and NIRS methods, and their application to young children, can be expected in the future.

Visuomotor Responses

Some aspects of visual development are intimately associated with specific visuomotor systems, and can be studied by recording how specific motor responses relate to visual stimulus configurations. For example, observation of the pattern and timing of saccadic eye movements can reveal the developing ability to shift fixation and shift attention (e.g., Atkinson, Hood, Wattam-Bell, & Braddick, 1992; Atkinson & Braddick, 2012); the development of smooth pursuit movements in response to motion can be determined by electro-oculographic (EOG) or optical recording of eye position (Aslin, 1981; von Hofsten & Rosander, 1997). Similarly, the response of adjusting focus (accommodation) to targets at different distances, and the overall refraction (focusing power) of the infant’s eyes can be assessed using optical measurements by photo- or videorefraction techniques (Braddick, Atkinson, French, & Howland, 1979; Hainline, Riddell, Grose-Fifer, & Abramov, 1992; Bharadwaj & Candy, 2009). The development of other visuomotor systems can be examined through infants’ visually guided reaching, grasping, and locomotion, either through simple observation of actions occurring in a particular visual context or by more quantitative instrumental measurements of the kinematic patterns (e.g., von Hofsten, Vishton, Spelke, Feng, & Rosander, 1998; Babinsky, Braddick, & Atkinson, 2012; Braddick & Atkinson, 2013).

Behavioral Vision Tests for Young Children

Specific tests, developed for assessment of visual function in young children, are discussed further below in the section on disorders of visual development. These tests include the ABCDEFV (Atkinson Battery of Child Development for Examining Functional Vision; Atkinson, Anker, Rae, Hughes, & Braddick, 2002a), a battery of short infant- and child- friendly portable sub-tests to make a general assessment of everyday functional vision (for ages from birth to six years, or equivalent mental ages). Other examples are tests for assessing specific aspects of visual cognition, such as TEA-Ch—Test of Everyday Attention in Children (Manly et al., 2001), and ECAB—Early Child Attention Battery (Breckenridge, Braddick, & Atkinson, 2013a; Breckenridge, Braddick, Anker, Woodhouse, & Atkinson, 2013b; Atkinson & Braddick, 2012), both measuring multiple components of attention and its deficits.

Different Components of Visual Development

Visual Acuity and Contrast Sensitivity

The most basic measure of developing visual function is acuity, the ability to register fine spatial detail. It can be assessed as the finest grating of black and white stripes (highest spatial frequency or smallest stripe width) which can elicit differential looking behavior compared to a uniform grey field matched in average intensity—or the finest grating for which changes can elicit a visual evoked potential. These methods indicate that the acuity of the one-month-old infant is between eight to twenty five times poorer than that of an adult, but show a very rapid development of visual acuity in the first months of life, with a more gradual development towards adult values for gratings by around three to four years (Dobson & Teller, 1978; Atkinson & Braddick, 1981b; Norcia & Tyler, 1985; Banks & Dannemiller, 1987). The ability to identify shapes from fine detail, as in the letter charts used to assess adult acuity, develops over a longer time course, to six to seven years. Typically developing young children, before six years of age, show “crowding,” that is, they have difficulty in identifying a letter if it is surrounded by nearby lines or other letters. This means that between three and six years of age, single letter identification may overestimate their functional acuity, and child-friendly “crowded” acuity tests, such as the Cambridge Crowding Cards (Atkinson, Anker, Evans, Hall, & Pimm-Smith, 1988a), should be used for children in this age range (or mental age range) to give a measure comparable to the acuity charts used to test adults.

A more general measure of visual detection of spatial pattern is the contrast sensitivity function, which plots the ability to register variations of light and dark over a range from broad scales (low spatial frequencies) to fine scales (high spatial frequencies). Visual acuity corresponds to the highest spatial frequency on this function, where maximum contrast is required to detect the grating. As for acuity, young infants’ sensitivity to contrast at low and medium spatial frequencies is also far below adult levels (Atkinson et al., 1974; Atkinson, Braddick, & Moar, 1977; Banks & Salapatek, 1978). However, the development is not uniform across this frequency range. In particular, adults and older infants show a drop in sensitivity for low compared to medium spatial frequencies, taken to reflect an accentuation in the response of visual neurons in the medium range caused by an opponent center-surround organization of receptive fields. This drop is not found in one-month-olds, suggesting changes in retinal organization in the first months of life.

Infants’ low acuity should be seen in functional perspective. High acuity is required for discerning visual details at large distances (e.g., hazards well ahead on the highway) or for very fine near tasks (e.g., reading small print or very delicate manual skills). These demands have little relevance in the visual ecology of the young infant, for whom significant visual events (e.g., interaction with a parent) are typically closer than one meter, and who lacks the motor control necessary for fine manual tasks. Thus, although typical one-month-olds would meet the legal criteria for blindness in an adult, they are sensitive to the visual information required to recognize faces and facial expressions at near distances. The key effect of viewing distance is emphasized by the detailed simulations of neonatal vision by von Hofsten et al. (2014).

Acuity and contrast sensitivity measures are important not only for what they tell us about the visual information available to the infant, but also for indications about underlying mechanisms. Acuity is potentially limited first by the quality of the optical image formed on the retina, secondly by the sensitivity and layout of the cone photoreceptors in the fovea, and thirdly by the performance of the neural networks transmitting spatial information from the eye to the brain. Optically, the infant’s eye is clear and usually reasonably well focused at the near distances used in testing. The photoreceptors are potentially a more significant limitation, since the thin, closely spaced cones which give adults high acuity in the fovea are short and stumpy, with a paucity of sensitive pigment and a wider spacing in young infants (Yuodelis & Hendrickson, 1986). These differences limit the infant’s acuity and sensitivity; however, calculations indicate that at most 25%–30% of the 12-fold acuity change from one month to adult can be attributed to changes in photoreceptor sensitivity and spacing, and they do not account for the changing shape of the contrast sensitivity function (Banks & Shannon, 1993). Thus, while receptor development has a significant role, the major change must occur beyond the receptors, in the organization of the neural pathways that transmit visual spatial information to the brain and its processing within the brain.

Refraction and Focusing

A sharply focused image on the retina depends first on the size and shape of the eyeball, which determines the basic “refraction” of the eye, and second on the accurate adjustment of the lens of the eye (accommodation). Young infants on average have a slightly hyperopic or “long sighted” refraction, but they adjust the lens so that in the first few months of life the infant’s eyes are usually focused on near objects around 40 cm; Braddick et al., 1979; Banks, 1980; Hainline, Riddell, Grose-Fifer, & Abramov, 1992; Horwood & Riddell, 2008). This is thought not to be a muscular limitation in the eyes, but rather an attentional limitation which is overcome for near objects by their large visual angle and, therefore, low spatial frequencies.

In the first months of life, infants are able to change their accommodation, but do not generally adjust it sufficiently for changes in target distance. While this will introduce blur, the neural and receptor limitations outlined above mean that infants’ acuity may be too low to distinguish the blurred from the sharp image. Thus it is likely that their acuity limits their ability to focus accurately, rather than vice versa (Atkinson & Braddick, 1981b).

Changes in refraction result from an active developmental process: animal models have shown that image blur acts as a stimulus to modulate the growth of the eye so that the blur is reduced, a process known as “emmetropization” (Howland, 1993; Wildsoet, 1997). However, this process sometimes fails to correct initial hyperopia (long-sightedness) and about 5% of Caucasian infants continue to show significant hyperopic refractive errors at twelve months of age (Atkinson, Braddick, Nardini, & Anker, 2007). Myopia (short-sightedness) is much more frequent in East Asian populations. In general, myopia increases from middle childhood onwards. This progression reflects in part the adaptive processes controlling eye growth, and can be exacerbated in some individuals by the persistent accommodation associated with visual near work (Adams & McBrien, 1992; Zadnik, 1997), a progression which appears to be counteracted by exposure to bright sunlight (Norton & Siegwart, 2013).

Many typically developing infants show significant levels of astigmatism in the first year of life, but within the process of emmetropization, these levels of astigmatism generally reduce to non-significant levels in most infants by two years of age (Atkinson, Braddick, & French, 1980).

Temporal Information in Infant Vision

As well as signaling the spatial pattern, the visual system must also signal changes over time, most importantly for registering movement. The analogy in time for acuity in space is the critical flicker frequency (CFF), the highest rate at which flicker can be detected. Infants’ cone photoreceptors respond electrically to rates as high as adults’ (Horsten & Winkelman, 1962) and even at one month, infants will show preferential looking towards a flickering field up to 40 Hz (Regal, 1981), about 70% of the adult limit (a striking contrast with the 20-fold change in spatial acuity). However, temporal processing is still very immature in contrast sensitivity and in detecting rapidly changing patterns (reviewed by Braddick & Atkinson, 2009). These results may be understood if the incomplete myelination of the infant’s visual pathway means that the transmission of neural signals from different retinal locations is poorly synchronized.

Vernier Acuity and Hyperacuity

Grating acuity assesses the ability to detect spatial detail, but this means little unless the spatial relationships within that detail are represented. Such a measure is “vernier acuity”—the ability to detect misalignment within a contour. Adults can judge this and other details that are smaller than the smallest separation that can be resolved in grating acuity, and so this is called a “hyperacuity” task, which requires the visual system to represent spatial relationships with high precision by accurately integrating information over an area, for example the contours around the break. Vernier acuity therefore provides an index of the development of pattern processing mechanisms that perform such integration.

Infants’ vernier acuity has been assessed by preferential looking towards grating stimuli that include vernier breaks, or through VEP responses to the appearance of such breaks (Manny, 1988; Skoczenski & Norcia, 1999). Direct comparisons of vernier with grating acuity show vernier performance increasing much more rapidly than grating acuity between two and six months (Shimojo, Birch, Gwiazda, & Held, 1984; Zanker, Mohn, Weber, Zeitler-Driess, & Fahle, 1992; Brown, 1997). These results, and similar findings on sensitivity to spatial phase relations between gratings (Braddick, Atkinson, & Wattam-Bell, 1986), suggest that over this age range, infants’ spatial vision improves in ways that go beyond a simple improvement in detection of spatial detail. There is an additional process which improves the infants’ ability to integrate this information into a representation of spatial relations. The vision of the youngest infants has some similarity to adults’ peripheral vision, where spatial judgments are particularly impaired relative to central foveal vision (Hilz, Rentschler, & Brettel, 1981; Stephenson, Knapp, & Braddick, 1991; Levi & Waugh, 1994). The rapid development of hyperacuity in the first year of life is followed by a relatively slow rate of improvement until adult levels are reached at around fourteen years of age, compared to parallel measurements of grating acuity which is mature by around six years of age (Skoczenski & Norcia, 2002).

Cortical Selectivity

According to the neurobiological model outlined above, visual development in the first postnatal months reflects the increasing role of processing mechanisms in visual cortex. Animal studies show that neurons in primary visual cortex (area V1) show highly selective responses, for example to contour orientation (Hubel & Wiesel, 1977), that are not apparent in the input to the cortex from the eyes. Development of this aspect of cortical processing can be assessed by the orientation-reversal VEP, a method designed to isolate orientation selectivity from lower-level responses to contrast. Such a response to an orientation change has been found in four to eight week olds but not in newborns (Braddick, Wattam-Bell, & Atkinson, 1986; Braddick, 1993). Behavioral tests show that discrimination of orientation is possible earlier (Slater, Morrison, & Rose, 1988; Atkinson, Hood, Wattam-Bell, Anker, & Tricklebank, 1988b) but the underlying mechanisms appears to have a sluggish temporal response, and cannot respond to the orientation changes at three per second and faster which are required for the VERP response (Hood, Atkinson, Braddick, & Wattam-Bell, 1992; Braddick, 1993). The cortical mechanism develops rapidly; interactions between cortical orientation detectors may be an important element in maturation (Morrone & Burr, 1986; Candy, Skoczenski, & Norcia, 2001). The orientation-reversal VEP, as well as being an index of normal visual cortical development, has proved to be a sensitive indicator of cortical function and deficit in the development of at-risk infants (Mercuri et al., 1996, 1998, 1999; Atkinson et al., 2008).

Motion Processing

Another feature of visual cortical cells is selectivity for different directions of motion. As for orientation, the development of cortical direction selectivity can be tested with VEP stimulus sequences that isolate responses to direction changes, an analogy to the orientation-reversal method outlined above. Like orientation selectivity, this cortical selectivity is not present in the newborn but appears as a VEP response around ten to twelve weeks (Wattam-Bell, 1991). These cortical processes do not emerge together; direction consistently lags orientation in development (Braddick, 1993; Braddick et al., 2005). Therefore, although characteristic visual cortical functions emerge in the first three months, this is a staged sequence rather than a unitary development, with binocularity, another cortical characteristic, emerging later still (see below). While all types of cortical selectivity must depend on the enormous increase in synaptic connections in visual cortex—about 10-fold between one to eight months (Huttenlocher, de Courten, Garey, & van der Loos, 1982)—the developmental processes that establish synaptic connectivity underlying orientation, directional, and binocular selectivity must be distinct.

Infants can be tested, using preferential looking or habituation, for discriminations that depend on detecting motion direction. These behavioral methods have demonstrated directional processing somewhat earlier than VEP measurements, but still find no directional selectivity before about seven weeks of age (Wattam-Bell, 1992, 1994, 1996a, 1996b; review by Braddick, Atkinson & Wattam-Bell, 2003).

Motion sensitivity underlies so many perceptual functions, that it is surprising that directional responses are not one of the earliest-developing features of vision. Motion processing must require some consistency in the timing of neural transmission to the cortex, to a greater degree than for processing of static pattern. This will depend on the progressive myelination of the visual pathway (Friede & Hu, 1967). It also depends on recognizing the sequence of stimulation between separate locations, which implies use of the horizontal connections linking cortical neurons which develop gradually in the first months (Burkhalter, Bernardo, & Charles, 1993). Infants’ sensitivity to fast velocities develops later than for mid velocities (Wattam-Bell, 1992, 1996a) suggesting a progressively increasing range of the underlying connections, seen also for binocularity (Wattam-Bell, 1999).

Even newborn infants show one significant directional response: the OKN response by which the eyes follow large patterned field motion (Dayton et al., 1964, Kremenitzer, Vaughan, Kurtzberg, & Dowling, 1979) (see video clip 1). However before two to three months, this depends on a wholly subcortical pathway with a characteristic monocular asymmetry (Atkinson & Braddick, 1981a; Braddick et al., 1992; Morrone, Atkinson, Cioni, Braddick, & Fiorentini, 1999). The different developmental course for OKN compared to direction-based preferential looking implies that different motion systems are involved (Mason, Braddick, & Wattam-Bell, 2003). Neonatal OKN, therefore, does not alter the conclusion that cortical motion processing only emerges after about six to eight weeks of age.

Video 1. A Three-Month-Old Infant Showing the Response of Optokinetic Nystagmus (OKN)—a Repetitive Pattern of Reflex Eye Movements, with Slow Tracking of the Motion in a Wide-Field Display, Interspersed with Rapid Saccadic Jumps in the Opposite Direction.

Higher Level Motion Processing

Sensitivity to motion serves a wide range of key perceptual functions—segmentation of differently moving objects and surfaces; information about 3-D structure, and about the observer’s motion through the environment; characteristic motion patterns of identifiable dynamic events, including causal sequences, and the “biological motion” patterns of other human beings. All these functions depend on processes that integrate local motion information to identify extended patterns. Local motions can be processed by the small directional receptive fields of areas V1 and V2, but much larger receptive fields are found in extrastriate motion-sensitive areas including V5 (also known as MT), MST, V3a, and V6. These latter areas are therefore the likely site of the integrative or “global” processes underlying motion-based perception. However, there are other areas in parietal and frontal lobes connected within the dorsal stream networks which may play a critical role in motion sensitivity tasks (as discussed below).

Global motion processes operate at an early stage of development. One index is the motion coherence threshold (Newsome & Paré, 1988)—the proportion of dots moving together within a random array which is needed to detect the common movement. Infants’ behavioral coherence thresholds show a rapid improvement over the weeks after direction discrimination first emerges (Wattam-Bell, 1994; Banton, Bertenthal, & Seaks, 1999; Mason et al., 2003). Global motion processing can also be demonstrated by VEPs which, by five months of age, show distinctive responses to the global organization of motion (Braddick & Atkinson, 2007; Wattam-Bell et al., 2010).

Infants can use motion information for several high-level perceptual discriminations. For example, infants can discriminate geometrical shapes that are defined only by motion segmentation (Kaufmann-Hayoz, Kaufmann, & Stucki, 1986), recognize them when later presented as static black and white shapes (Johnson & Mason, 2002), and use them to define occlusion relationships (Johnson & Aslin, 1998); discriminate 3-D objects using dot patterns representing their surfaces in motion (Arterberry & Yonas, 1988, 2000); and link the parts of a partially occluded object by their common motion (Kellman & Spelke, 1983). They recognize the dynamics of casual event sequences (Leslie, 1984; Wickelgren & Bingham, 2001) and sequences with simple shapes that adults perceive as social interactions (Rochat, Morgan, & Carpenter, 1997). Infants are also sensitive to patterns of point-light motion that characterize biological motion (Fox & McDaniel, 1982; Bertenthal, Proffitt, & Cutting, 1984; Bertenthal, Proffitt, Spetner, & Thomas, 1985; Booth, Pinto, & Bertenthal, 2002). Most of these tests have been with three to six month old infants, and so are consistent with an emergence of directional motion sensitivity after seven weeks of age, but they demonstrate that, within a few weeks, infants become able to integrate directional information into global representations that serve complex perceptual functions.

It may be speculated that this integration is based on the connectivity between V1 and extrastriate areas including MT/V5, and that at least a crude form of this connectivity exists very early, awaiting the development of local directional selectivity in V1. fMRI studies (Biagi et al., 2015) show that MT/V5 is already activated by motion in seven-to-ten-week-old infants, with a network of connectivity between motion areas. Global motion responses in five-month olds’ extrastriate areas are also evidenced by VERP experiments (Wattam-Bell et al, 2010), which also show that global motion and global form are processed by anatomically distinct systems, although these networks are substantially reorganized between infancy and adulthood.

Processing of Global Static Form and Global Motion Compared

The brain areas processing global motion (V5, V3a, and others) are parts of the extrastriate dorsal stream, while global processing of static pattern or object form is largely a function of the ventral stream (although this division is far from complete—see Perry & Fallah, 2014; Gilaie-Dotan, 2016) The two streams can be compared using closely analogous stimuli, in which the infant or young child must detect the coherent organization of moving dots (dorsal task) or short line segments into concentric circles (ventral task), amongst “noise” introduced by randomizing the orientation of some motion paths or line segments—the “Ball in the Grass” test (Figure 2). In infancy, despite the delay of motion discrimination compared to local orientation, responses to global motion are established before those to form (Braddick & Atkinson, 2007; Wattam-Bell et al., 2010). Yet, when coherence thresholds for form and motion are tracked through childhood, motion thresholds are worse and more variable than form thresholds for four-year-olds, and take longer to reach adult values (Gunn et al., 2002; Atkinson & Braddick, 2005, Braddick et al., 2016a). However, this developmental trajectory depends on parameters such as speed, density, and spatio-temporal intervals (Meier & Giaschi, 2014; Hadad, Schwartz, Maurer, & Lewis, 2015), with the reported age at which mature motion performance is reached ranging from three years to adolescence.

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Figure 2. The “Ball in the Grass” Test for Comparing Children’s Sensitivity to Global Motion Coherence and Global Form Coherence, Described in Detail in Braddick et al. (2016a, 2016b). (A) motion test pattern, with the target on the right. Trajectories of dots are indicated by red arrows. The boundary of the “ball,” shown by the red dashed line, was not present on the screen. (B) form test pattern, with target (100% coherence) on the left. (C) child performing the form coherence test on a laptop screen. (D) graded series of global form patterns. In the test, the coherence level is adjusted by an adaptive procedure to estimate the threshold at which the child can identify the side containing the global structure, at a level of 75% correct. The graded series of global motion patterns, with the same coherence values as in D, are shown in Video 2.

Children’s individual variability in motion coherence thresholds may provide a clue to underlying neural networks. These thresholds (but not equivalent form thresholds) have recently been shown to relate to structural differences in the area of the parietal lobe and in the superior longitudinal fasciculus (SLF), a major fiber tract between parietal and frontal lobes (Braddick et al., 2016a, 2016b). These relationships suggest that the limiting factors may not be in the extrastriate areas that integrate local motion signals, but rather in attention and decision-making processes that are involved in global motion but not form detection.

Furthermore, good motion coherence sensitivity (but not necessarily good form sensitivity), was shown to correlate with good performance on tasks of visual-motor integration and numerical cognition in the same children (Braddick et al., 2016a). These tasks are known to involve parietal lobe processes (e.g., Dehaene, Piazza, Pinel, & Cohen, 2003; Price, Holloway, Räsänen, Vesterinen, & Ansari, 2007; Butterworth, Varma, & Laurillard, 2011; Ranpura et al, 2013), suggesting that they share, with motion processing, some common neural underpinnings between parietal and frontal lobes. Atkinson (2017) suggests that this parietofrontal network may be related to the multiple demand (MD) network, identified in adults, underpinning processing in tests of “fluid intelligence” (Duncan, 2010; Mitchell et al, 2016).

The long developmental course of global motion sensitivity, and its associations with other parietal functions, may reflect its role as a signature of “dorsal stream vulnerability” in developmental disorders, discussed in a later section of this paper.

Video 2. Global Rotary Motion Displays with Five Progressive Levels of Coherence Between 0%–100%, as Shown for Global Form Coherence in Figure 2D (see caption for Figure 2).

Development of Binocularity

Binocular interaction is a third signature of specifically cortical processing. This interaction allows the detection of binocular disparity, the basis for stereoscopic depth perception.

Infants can be tested with a “random-dot correlogram” in which dynamic dot patterns presented separately to the two eyes are alternately correlated and anti-correlated. Each eye separately sees only a randomly changing dot pattern, so a VEP response is a signature of binocular interaction in the cortex. This first emerges around eleven to sixteen weeks, although with considerable individual variation (Braddick et al., 1980; Petrig, Julesz, Kropfl, Baumgartner, & Anliker, 1981; Braddick, Wattam-Bell, Day, & Atkinson, 1983; Wattam-Bell et al., 1987). A number of behavioral methods also indicate that infants from about four months are sensitive to stereo disparity (Fox, Aslin, Shea, & Dumais, 1980; Held, Birch, & Gwiazda, 1980; Birch, Gwiazda, & Held, 1982; Birch, 1993).

Binocular vision depends on the two eyes accurately converging on the target. The emergence of binocular responses might therefore depend on the development of oculomotor control. However, young infants generally maintain accurate vergence and adjust it for target distance (Aslin, 1993; Hainline & Riddell, 1995). Furthermore, infants’ measured binocularity is not improved when tested in ways that do not depend on vergence accuracy (; Birch, Gwiazda, & Held, 1983; Birch & Stager, 1985; Birch, 1993).

The development of functional binocular vision, then, depends on establishing binocular connectivity in the cortex rather than on eye alignment. Indeed, the robust maintenance of accurate alignment is likely to depend on cortical mechanisms signaling small deviations between the two eyes’ images. This feedback loop fails in strabismus (persistent misalignment of the two eyes), as discussed later in this article.

3-D Shape and Depth Perception

Binocular disparity is only one source of information enabling the perception of distance, surface slant, and solid shape. As well as structure from motion (motion parallax) and binocular disparity, there are the so-called “pictorial” cues that can be seen monocularly, including interposition of a far surface by a nearer one, shape from shading, linear perspective, and gradients of texture density.

Distance information is necessary for perceiving the invariance of objects from different viewpoints (size and shape constancy). Findings of size or shape constancy in newborns (Slater, Mattock, & Brown, 1990) and three-to-four-month-olds (Caron et al., 1979; Granrud, 2006) imply that infants had a source of visual distance information, but these findings do not identify what that source is.

3-D structure may look distinctive to an infant, but does it truly signify depth? Yonas, Arterberry, and Granrud (1987) demonstrated that four-month-old infants transferred recognition of a motion-defined 3-D shape to a static stereo version of the same shape. But the most direct test of depth “meaning” is its relation to motor actions. Prisms distorting the distance at which the eyes had to converge on an object produce concomitant changes in four-to-seven-month-olds’ reaching behavior (Von Hofsten, 1977), as does occlusion of one eye (Braddick & Atkinson, 2013). Depth perception can also be assessed through infants’ preference for reaching to the apparently nearer object. This approach has shown infants to be sensitive to a range of monocular depth cues: interposition signaled by boundary continuity (Granrud & Yonas, 1984); linear perspective and texture gradient (Yonas, Granrud, Arterberry, & Hanson, 1986); shading of a concave solid form (Granrud, Yonas, & Opland, 1985); relative size of objects (Yonas, Granrud, & Pettersen, 1985); and the linked motion of surface texture and its boundary (Craton & Yonas, 1988). These preferences are related to depth, since they can be overridden by binocular information that shows the display is flat (Granrud et al., 1985). However, the pictorial cues are effective only for seven-month-old infants, not at five months, a transition which can be tracked longitudinally (Yonas, Elieff, & Arterberry, 2002).

These findings imply a developmental sequence in the use of depth cues to guide behavior. It is plausible that the information from image motion and binocular disparity, available from three to five months, can provide a scaffolding from which the infant later learns correlations with the more complex and variable pictorial cues based on perspective and shading in the same scenes. There does not yet appear to be any positive evidence for such a developmental model, although it might be possible to test it in children who have only one functional eye from birth. By whatever route, before 12 months the infant has access to a three-dimensionally organized representation of space, which can serve the dorsal-stream systems guiding reaching and locomotion, and ventral stream systems for recognizing solid shape. However, the ability to combine sources of distance information efficiently is a more prolonged developmental process, which is not adult-like until at least eight years (Nardini, Bedford, & Mareschal, 2010; Dekker et al, 2015).

Segmentation and Figure-Ground

Visual objects are rarely isolated but overlay one another in the images of cluttered visual scenes. An essential part of visual perception therefore is segmentation, defining boundaries so that an object can be separately processed. These boundaries may be defined by luminance contrast, but often need to be derived from differences in surface texture, motion, or stereo depth (Peterhans & von der Heydt, 1991). Can infants detect such boundaries, and can they operate visually on the segmented objects that result?

Relative motion is a powerful cue for segmentation. Its use is shown by Wattam-Bell’s (1992, 1994) work on two-month-old infants’ preference for a region containing oppositely moving strips, and by three-month-olds’ ability to identify shapes defined by their motion against the background (Kaufmann-Hayoz et al., 1986). Boundaries can also be defined by the aligned terminators which occur where contours on a surface are interrupted by a nearer surface; infants as young as two months can detect such boundaries (Curran, Braddick, Atkinson, Wattam-Bell, & Andrew, 1999). A related effect occurs in figures such as the well-known Kanisza triangle, where aligned corners create, for adults, a “subjective contour” bounding an occluding object. By three to four months of age in dynamic displays, and somewhat later in static displays, infants are sensitive to the presence of such alignments (Ghim, 1990; Yonas, Gentile, & Condry, 1991; Kavsek, 2002; Otsuka & Yamaguchi, 2003; Kavsek & Yonas, 2006). Two-month-olds are also sensitive to the segmentation by texture differences between an object and its background (Atkinson & Braddick, 1992; Sireteanu & Rieth, 1992), although segmentation by motion appears to be a stronger effect, and may serve as the developmental foundation for other means of segmentation and grouping.

When a visual boundary divides two regions, adults perceive one of them as “figure,” whose shape is defined by the boundary, and the other as “ground” which is not linked to the boundary (see for example in adults, Driver & Baylis, 1996) There is little evidence on how infants develop this sense of figure and background. However, Craton (1989; reported in Arterberry, Craton, & Yonas, 1993) showed that kinetic information (texture accretion and deletion, which can define the nearer of two regions), determined which region formed a shape that five-month-old infants could subsequently recognize. Such a motion-defined shape can also determine a five-month-old’s target for reaching (von Hofsten & Spelke, 1985). It appears, then, that grouping and segregation based on motion serve to define figure and ground for infants before six months of age, and may act as scaffolding for other cues for segmentation, as we have suggested for depth information.

Visual Face Processing

Faces are stimuli of great importance to the developing child as the major source of social communication and establishing human relationships, and the processing and recognition of faces in adults appears to be served by a specialized cortical system, particularly in the fusiform gyrus (Kanwisher, 2000). There is consistent evidence that newborn infants are specifically sensitive to some basic aspect of the configuration of facial features (Goren, Sarty, & Wu, 1975; Johnson et al., 1991; Johnson & Morton, 1991; Simion et al., 1998) or at least have visual preferences which bias them to acquire face-related information (Turati, 2004), at an age before the onset of visual cortical functions. Johnson and Morton (1991) proposed a model in which a subcortical “CONSPEC” mechanism determined initial newborn fixation biases towards face-like stimuli, which aided the establishment of specialized cortical circuits for face processing (which they termed “CONLERN”). Indeed faces occur with very high frequency in the field of view in the first months (Fausey, Jayaraman, & Smith, 2016). There remains some controversy concerning whether the visual properties which trigger CONSPEC are face-specific, with an alternative hypothesis being that the trigger is high contrast detail in the upper rather than lower visual field (Simion et al., 2011). This idea would explain why an inverted triangle of three high contrast blobs does not trigger the CONSPEC mechanism, whereas the upright three-blobs stimulus does.

The idea of the CONSPEC mechanism has recently been updated by findings of a pathway which bypasses visual cortex to connect superior colliculus through the pulvinar nucleus to the amygdala. There is good evidence that this pathway can mediate responses to facial expressions in patients with cortical lesions (Morris, De Gelder, Weiskrantz, & Dolan, 2001) and it has been argued as a basis for neonatal face processing (Johnson et al., 2015). However, the role of this subcortical pathway in infant development, in particular whether the pulvinar is functioning at birth and its relationship to cortical processing, still remains speculative. Event-related potential (ERP) responses showing face-specificity can be seen in infants by four months of age (de Heering & Rossion, 2015). However, face-related ERPs appear to be less specific in infants than adults (de Haan, Johnson, & Halit, 2003). fMRI also shows the origins in infancy of face specialization in the fusiform area, but again the specificity is rudimentary compared to the adult brain (Deen et al., 2017).

Beyond the simple detection of a face configuration, infants can use face information in more complex discriminations. For example, soon after birth they show behavioral discrimination between their mother’s face versus a stranger (Bushnell et al., 1989). However, in the first weeks, infants’ face recognition is heavily dependent on the outer contour of the face rather than internal facial features (Bushnell, 1982; Turati, Macchi Cassia, Simion, & Leo, 2006). Some discrimination of emotional expressions can be demonstrated at three months (Barrera & Maurer, 1981), although full sensitivity to expressions appears to have quite prolonged development (Caron, Caron, & Myers, 1982, 1985; Nelson, 1987). Abilities of facial discrimination become “narrowed” to specifically human characteristics during infancy: six-month-olds will recognize monkey individuals as well as humans, but nine-month-olds do not (Pascalis, de Haan, & Nelson, 2002), and a similar narrowing occurs towards faces of a familiar racial group (Kelly et al., 2007).

Color Vision

Color is a vivid component of our visual experience, and is important for segmenting scenes and recognizing objects and surface materials. There is evidence that a distinctive color does “pop out” of an array for four-month-old infants (Gerhardstein, Renner, & Rovee-Collier, 1999; Franklin, Pilling, & Davies, 2005). Color information is derived from comparing the signals from long-, medium-, and short-wavelength (L, M, & S) cone photoreceptors. The light-sensitive pigments that distinguish these receptors are present early in fetal life (Xiao & Hendrickson, 2000), and responses depending on each class can be demonstrated at four weeks of age (Knoblauch, Bieber, & Werner, 1998). However, infants’ color vision depends on the sensitivity of these cone receptors, and receptor immaturity is a limit on color vision just as it is on acuity and contrast sensitivity (Brown, 1990; Banks & Shannon, 1993). So, while color-based discriminations are very weak in infants before about two months, this does not necessarily imply that there is a specific immaturity of color mechanisms as such.

As for acuity, the neural mechanisms that compare the signals also have to mature. However, by two months infants clearly show discrimination based on the red-green axis derived from comparing L and M cones (Peeples & Teller, 1975; Hamer, Alexander, & Teller, 1982; Morrone, Burr, & Fiorentini, 1993; Crognale, 2002). (It is important to demonstrate that their behavior is not based on brightness differences, which is technically demanding since infants’ luminance matches are not necessarily the same as adults’.)

There is some evidence of a lag in development of color responses that depend on the S- (“blue”) cones: two-month-olds make eye movements following moving color gratings that can be detected through L- and M-cone signals, but no such eye movements are seen, even in four-month-old infants, for gratings whose visibility depends on the S-cones (Teller, Brooks, & Palmer, 1997). The later development of color discrimination based on the S-cones may reflect the fact that these cones do not send information to the superior colliculus (Schiller & Malpeli, 1977; Leh, Mullen, & Ptito, 2006), with development depending on of the increasing role of cortical processing in the first months of life. Even for the L- and M-cones, color discrimination improves sharply relative to luminance contrast discrimination between three to four months, possibly reflecting the development of a specific cortical color system (Dobkins, Anderson, & Kelly, 2001).

Studies measuring color preferences have shown that given a choice, infants prefer to look at red and purple colors compared to yellow and green (Brown & Lindsey, 2013). This requires them to use color rather than luminance differences. However, these apparent preferences may simply reflect the distinctiveness of these colors from their background, rather than any affective preference. It has been suggested that infants prefer the basic color categories (red, yellow, green, blue) over “secondary” colors (Bornstein, 1975; Franklin et al., 2008). This result has been hard to demonstrate convincingly at this age, although results from a recent study have identified neural correlates for color categories in five to seven month old infants (Yang et al., 2016).

Action Modules in the Dorsal Stream

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Figure 3. A Simplified and Updated Version of a Scheme First Published by Atkinson (2000), Summarizing Dorsal Stream Connections of Visuomotor Modules for Control of Four Behaviors—Arm Movements for Reaching, Hand Movements for Grasping, Saccadic Eye Movements, and Smooth Pursuit Eye Movements, and their Relationship to the Control of Spatial Attention. Dorsal-stream brain areas are shown in blue, ventral-stream in brown, and black are subcortical areas. Areas which have been shown to be involved in the spatial direction of attention are highlighted in green. Networks shown are based on primate studies and human neuropsychology (data reviewed by Jeannerod, 1988; Milner & Goodale, 1995; Rizzolatti, Fogassi, & Gallese, 1997; and Galletti et al., 2001).

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Figure 4. A Schematic Illustration (Atkinson & Braddick, 2011) of the Scheme Proposed by Kravitz et al. (2011) for Three Networks of the Dorsal Stream with Distinct Functional Roles, Shown as Three Horizontal Bands Separated by Dashed Horizontals. The scheme has been drawn to allow direct comparison with the visuomotor modules suggested in Figure 3. In Kravitz’s scheme, the modules for manual actions come within the “parieto-premotor circuit” (a, middle strip of the figure) subserving action control, and those for oculomotor actions within the “parieto-prefrontal circuit” (b, lower strip) involved in spatial memory and attentional control. The third “parieto-medial temporal” pathway (c) involves interaction with the ventral stream in the parahippocampal cortex and hippocampus and is proposed to be involved in spatial navigation. However, this diagram is not intended as a comprehensive chart of the connections of the areas shown—for example it omits connections with the superior temporal sulcus where motion information interacts with the ventral stream in biological motion—a function not discussed in this review. Abbreviations as for Figure 3. Additional abbreviation: EF = executive function.

The model of Figure 1 indicated the relationship to developing neural systems of major visuomotor milestones: exploratory head and eye movements, directed reaching and grasping, and locomotion. Each involves a distinct visuomotor module within the dorsal stream, requiring spatial representations at different scales and with different frames of reference. For reaching and grasping the infant only needs to represent space near the body in an egocentric reference frame relating object locations to hand actions. For locomotion, the child needs to represent the larger scale environment on a scale beyond arm’s length, and with a reference frame that remains stable in space as the body moves. There has been extensive behavioral work on this progression of visuomotor control for posture, manual actions, and locomotion, through infancy and early childhood (recently reviewed by Adolph & Franchak, 2017).

Figure 3 shows a schematic model of some of these dorsal stream modules which need to develop in infants and children to reach maturity. This schematic draws on extensive reviews of neuropsychology on adult patients and studies of the primate brain (Milner & Goodale, 1995; Jeannerod, 1997; Rizzolatti, Fogassi, & Gallese, 1997; Galletti et al., 2001). It shows how distinct pathways within the dorsal stream provide the visual information for control of different manual and oculomotor actions. It also highlights how areas within these pathways (highlighted in green) are those that have been found to play a role in the spatial direction of attention (Miller & Buschman, 2013; Szczepanski, Pinsk, Douglas, Kastner, & Saalmann, 2013).

This scheme can be extended to a wider range of functions where we have used a recent analysis of the anatomy of the dorsal stream and its projections in the adult brain (Kravitz, Saleem, Baker, & Mishkin, 2011), which shows three major branches illustrated schematically in Figure 4. Branch (a) connects parietal areas to premotor cortex, and includes the visuomotor modules for the guidance of manual actions outlined in Figure 3. A second branch (b) connects to the frontal eye fields and prefrontal areas underpinning spatial memory and attention; and a third pathway (c) connecting to medial temporal lobe and hippocampus, is involved in delivering spatial information and integrating it with information from the ventral stream for navigation and topographic cognition. Developmental aspects of each of these three functions are discussed below.

Head and Eye Movements Linked to Visual Attention

Eye movement systems are the first action modules to develop, controlling saccadic tracking and smooth pursuit of objects of interest, and saccades and head movements to switch attention between objects. These cannot be considered separately from the mechanisms controlling attention, as attention is often considered as a mechanism of “selection for action,” whether the action is a saccade to fixate an object, or a bodily movement such as a reach directed towards it (Rizzolatti, Riggio, Dascola, & Umiltá, 1987; Berthoz, 1996). Figure 3 highlights areas involved in selective attention that overlap with dorsal-stream action circuits.

The superior colliculus in the midbrain combines a visual map with one directing eye movements through the oculomotor nuclei. This provides an orienting system which can direct attention to significant changes in the world, and which is functional from birth. The superior colliculus generates saccades—standardized jerky eye movements whose dynamics are largely adult-like from birth (Hainline, Turkel, Abramov, Lemerise, & Harris, 1984), although they are not initially well calibrated to land exactly on the target (Aslin & Salapatek, 1975).

This system has been studied using the “Fixation Shift Paradigm” in which the infant initially fixates one target and then a saccadic eye movement is elicited by a second target appearing on the left or right (e.g., Atkinson, Hood, Wattam-Bell, & Braddick, 1988c; Atkinson et al., 1992; Atkinson & Braddick, 2012; Kulke, Atkinson, & Braddick, 2015). Infants before two months of age make such shifts much less readily if the original target remains visible (“competition”) than if it disappears when the second target appears (“non-competition”). It is proposed that shifts in non-competition can be initiated by a subcortical circuit through the colliculus, but that competition requires modulation of this circuit by a cortical pathway to disengage reflex fixation on the central target. The development of prompt fixation shifts under competition suggests that this cortical system becomes functional around two to four months of age in typically developing infants (Atkinson et al., 1992; Atkinson & Hood, 1997). The development of this modulation by the cortex can be mapped out by varying the interval between offset of one target and onset of another in, for example, the “Gap-Overlap paradigm” (Hood & Atkinson, 1993; Csibra, Johnson, & Tucker, 1997). In studies using EEG, frontal cortical areas including the frontal eye fields have been identified as a possible source of the developing control of disengagement (Csibra, Tucker, & Johnson, 1998), with a shift in laterality over the first year of life (Kulke, Atkinson, & Braddick, 2017).

This necessity of a functioning cortex for disengagement in the fixations shift paradigm was first demonstrated by tests on two young infants with one cerebral hemisphere surgically removed (hemispherectomy) to treat intractable epilepsy. These infants could shift to fixate a non-competing target on either side of the central target, but could not shift fixation, under competition, to the side of visual field served by (contralateral to) the absent hemisphere (Braddick et al., 1992).

Fixation shift deficits, including “sticky fixation” when the infant cannot disengage, are characteristic of infants with perinatal brain damage, even when damage is less severe than hemispherectomy (e.g., Hood & Atkinson, 1990; Mercuri et al., 1996, 1997a, 1997b, 1999; Atkinson & Hood, 1997). Additionally, infants’ delay or failure in fixation shifts under competition has been shown to be a predictor of later neurological outcome (Mercuri et al., 1999; Atkinson et al., 2008).

Action Systems for Eye Movement Control: OKN and Smooth Pursuit

A basic visual spatial action system is required to track moving objects and people, and to stabilize objects on the retina. Its earliest form is optokinetic nystagmus (OKN), responding to movement of a large textured field. This reflexive image-stabilization system depends on a subcortical circuit involving the nucleus of the optic tract. This circuit is operating in newborns and has a characteristic signature that in monocular viewing with the left eye, only left-to-right image motion can drive eye movement, and conversely for the right eye. As discussed earlier, it uses motion information which apparently is not available to other perceptual systems. The developing symmetry of OKN in both directions depends on cortical circuits associated with binocularity, as evidenced by its absence in hemispherectomized children (Braddick et al., 1992; Morrone et al., 1999) and in individuals with deficient binocularity, often related to strabismus (Atkinson & Braddick, 1981a; van Hof-van Duin & Mohn, 1986).

Smooth pursuit eye movements resemble the slow phase of OKN. However, the ability to pursue a small target moving across a background must reflect an ability to select the target and inhibit the OKN responses which would tend to stabilize the eyes on the background: the development of eye movements that can smoothly pursue such a target therefore must reflect an ability to select the target and register its motion. Before two months, moving targets are generally followed by a series of jerky refixations, with episodes of smooth pursuit increasing from two months of age onwards (Aslin, 1981). This is consistent with pursuit depending on cortical directional mechanisms, which emerge around the same age. However, for large slowly moving targets, episodes of pursuit occur even at one month or younger (Hainline, 1993; von Hofsten & Rosander, 1996, 1997; Phillips, Finocchio, Ong, & Fuchs, 1997). OKN and pursuit mechanisms serve overlapping goals, and there appears to be developmental continuity between them.

The development of pursuit illustrates some more complex aspects of visuomotor control. For example, infants show some predictive tracking, anticipating the reversals of a regularly oscillating target (von Hofsten & Rosander, 1996; Rosander, 2007). This shows that the newly developing visuomotor module for pursuit can link to a learning mechanism which engages an anticipatory motor program; a process believed to involve the cerebellum (Rosander, 2007). Predictive tracking also occurs when infants anticipate where and when a moving object will emerge from behind an occluder (reviewed by von Hofsten, 2005).

Visually Guided Reaching and Grasping

Two important visuomotor modules control the visual guidance of reaching and grasping. It is controversial how far the crude “pre-reaches” in the first months of life are visually directed responses, and how far they reflect a non-specific response to the general direction of attention (see von Hofsten, 1982, 1984, 1991). Successful reaching and grasping of objects within arm’s length usually emerges between four to six months of age. The action systems involved must use visual information both about the object’s direction and distance, and whether its size and shape make it a suitable target, graspable by the infant’s hand. The visuomotor modules engaged in this development are discussed in Atkinson and Braddick (2003) and Braddick and Atkinson (2013).

Visually guided reaching develops at a similar age as binocularity, around four months. Evidence that binocular disparity information is initially a key input to the visuomotor module for reaching, followed by other cues for distance, is discussed above in relation to the development of depth perception.

At age six to nine months, infants often reach quite compulsively for small objects presented within arm’s length. Initially, this action is closely coupled to the orienting system, and given a choice infants will tend to reach for the more salient, that is the larger, of two objects (Newman, Atkinson, & Braddick, 2001). However, somewhat later, the computation of “graspability” develops, which is thought to be a function of area AIP (see the grasping module in Figure 3) and feeds into the mechanism for selection of targets for reaching. This behavior raises the question of the visual information by which an infant determines that an object is graspable and hence a suitable target for reaching. Infants who compulsively reach at this age do not necessarily show the pre-shaping of the hand, which leads to the grasp aperture during the reach being calibrated to the object size.

The visuomotor modules used for successful reaching and grasping have been investigated in experiments which combine preferential looking with preferential reaching (Newman et al., 2001). In preferential looking infants make an orienting response of head and eyes towards the most salient object or region in the visual field—a function of luminance, color, motion, depth and contrast, and of the spatial structure of the object. The computation of salience, so defined, is characteristic of the cortical modules which contribute to the orienting system (providing output through the superior colliculus). When an infant is presented with two solid objects, similar in shape and surface properties, the infant tends to orient to the larger object (Newman et al., 2001).

However, reaching is only an appropriate action for objects in the size range which can be grasped. Computation of size is not necessarily possible for the infant at the age when the motor schema of reaching becomes available, but when it is possible, reaching will be preferentially directed to the smaller object of a pair, when the larger is beyond the span of the infant’s hand. The form of the action may also be affected by these visual properties. Braddick and Atkinson (2007, 2013) examined reaches to a wide range of object sizes (three to 46 cm) and found that, at different ages, size determined the incidence of bimanual reaches and of “non-grasp contact” in which the infants pushed or palpated the surface of large objects. Thus visual size determines not just the initiation of a manual action but also its kinematic form, with distinct action patterns for “grasp object” and “explore surface.” At later ages infants use more subtle visual “affordances”—for example, information about the expected rigidity of an object (Barrett, Traupman, & Needham, 2008) and how its symmetry will affect grasp stability (Barrett & Needham, 2008), to determine their actions.

These specific uses of visual information suggest that the two visuomotor dorsal stream systems, for orienting and for reaching, may be driven by different visual information from the same objects. The studies of Newman et al. (2001) have shown they interact differently at different ages (Atkinson & Braddick, 2003). When infants first start to reach (up to around eight months), they do not show a significant reaching preference based on size, but their reaching is predominantly directed to the object they initially fixate. We can infer that the visual processing of “graspability” is not yet linked into a visuomotor module for reaching, but that there is a substantial coupling between the systems which control reaching and orienting. Between eight to twelve months a strong preference emerges for reaching for the smaller, graspable object. Infants at this age show a decoupling of reaching and initial visual orienting—they are more likely than younger or older infants to first fixate one object and then reach for the other if its size is more appropriate for grasping. This decoupling can be emphasized by manipulating visual salience: a schematic face on one object increases the visual preference for looking, without altering its “graspability” and hence without a corresponding increase in the tendency for it to elicit reaching in competition (Newman et al., 2001). After twelve months of age, reaching becomes less selective towards the smaller object, (perhaps because the infant’s grasp can encompass larger objects) while reaching and initial looking become more congruent again. It appears that, by this age, the orienting and reaching systems have been integrated into a single piece of goal-directed behavior.

End State Planning

Visual information is used in two ways in guiding action. We have discussed how visual information can determine the selection of a target for reaching and grasping, and can modulate the form of that action. Actions also require planning, for example anticipating the end-state—the position of the limb in which an action will leave the motor system. For example, an object such as a vertical handle which is to be rotated clockwise with the right hand requires a different orientation of the grasp (thumb-down) from one to be rotated anti-clockwise (thumb up), if the final position of the wrist is to be comfortable (Rosenbaum, Vaughan, Barnes, & Jorgensen, 1992). Such end-state planning is likely to involve the integration of dorsal stream information with pre-frontal areas involved in inhibiting inappropriate actions and coordinating the elements of action sequences. Children aged about four years tend to follow a strategy in which grasp is determined by the immediate characteristics of the object, but by seven to eight years children move to adult-like end-state planning (Smyth & Mason, 1997). Children with Williams syndrome (WS), in contrast, continue to use the younger strategy or more stereotyped actions (Newman, 2001; Braddick & Atkinson, 2013). WS is associated with a dorsal stream deficit (Atkinson et al., 1997) but this failure suggests that the interchange of information between dorsal-stream and frontal systems is an important aspect of the deficit (Atkinson, Braddick, Anker, Curran, & Andrew, 2003).

Action Modules for Locomotion

Locomotion becomes part of the infant’s behavioral repertoire around the end of the first year. It requires information to be registered from far space, although this must be integrated with more local frames of reference when, for example, walking or crawling brings a desired object into range as a reaching target. Vision, as well as defining the direction of locomotion towards a target, must also provide the information about obstacles, surfaces, and gradients which determine whether a chosen route affords locomotion. The classic example of such information comes from the “visual cliff” studies of Gibson and Walk (1960) which showed that crawling infants avoid a visual depth difference (probably signaled by motion parallax and/or texture perspective). More recent studies have shown sensitivity of infants’ locomotor choices to visual information about gaps, obstacles, supports, and slopes (Berger & Adolph, 2007).

Locomotor skills are acquired over a long period; for example, stair descent remains immature for several years (partly because the dimensions of the built environment are not adapted to young children). However, it has been shown that the adult ability to use visual information about stair depth to calibrate leg movements even before touching down on the first step is already present, and calibrated to leg length, in children as young as three years (Cowie, Braddick, & Atkinson, 2008; Cowie, Atkinson, & Braddick, 2010).

Attention and Executive Functions

Attention has already been discussed above in the context of spatial orienting and target selection in early infancy using measures such as the Fixation Shift Paradigm. Shifts of visual attention can be overt, as when eye movements are directed to the source of interest, or covert, as in cases where gaze is maintained at one location, yet the focus of attention shifts to another location. Inhibitory attentional processes can be demonstrated in the phenomenon called “Inhibition of Return.” If attention is oriented to a peripheral location by a visual cue and returns to a central fixation point, processing of subsequent targets at that location is inhibited relative to targets in the contralateral position. By six months of age typically developing infants are able to readily shift overt attention between objects when more than one object is visible at the same time. In addition, six-month-olds, but not three-month-olds, show covert attention shifts in “Inhibition of Return” (Hood, 1993). In this study six-month-olds’ saccadic latencies to targets appearing at the same peripheral location were longer than latencies to targets appearing at the contralateral position, even though no eye movement had been made to the cue.

Attention is not a unitary function. Neuropsychological analyses distinguish neural systems controlling (a) selective attention, (b) maintenance of sustained attention, and (c) attentional control systems (executive function) that are involved in planning behavior, maintaining current goals and sub-goals, and inhibiting prepotent but inappropriate actions (Posner & Petersen, 1990). There is some evidence that the developmental trajectories of these components differ, with earlier maturity in selective attention (before six to seven years) contrasting with the continued development of sustained attention into adolescence, and rapid development of executive functions between seven and eleven years (e.g., McKay, Halperin, Schwartz, & Sharma, 1994; Rueda et al., 2004; Kelly, 2000) with development extending through adolescence. The TEA-Ch test battery provides evidence that these components can be dissociated psychometrically in school age children (Manly et al., 2001). In the Early Child Attention Battery (ECAB), adapted for children aged three to six years, these components are found not to be dissociated in the youngest children, but become so in the latter half of this age range, that is, after age four years (Breckenridge et al., 2013a). The ECAB subtests can be used to define an individual attention profile across selective, sustained and executive control components in both the visual and verbal domains. As discussed below, this allows different developmental disorders to be characterized in terms of specific attention deficits.

Executive function is relevant to the action planning discussed above. Prefrontal cortex, especially the dorsolateral prefrontal cortex, plays a key role in this kind of behavior. A number of tasks have been developed to examine executive function in preschool children (e.g., Hughes & Russell, 1993; Gerstadt, Hong, & Diamond, 1994; Hood, 1995; Backen-Jones, Rothbart, & Posner, 2003; Kirkham, Cruess, & Diamond, 2003; see Carlson, Zelazo, & Faja, 2013, for a review); these show significant changes in the ability to inhibit prepotent responses, and control attention flexibly, between the ages of three and four years.

Executive function has an important role in the control of visuo-spatial behavior. A sensitive test of response inhibition for adults is the “anti-saccade” task, in which subjects are required to move their eyes away from a target which appears (Everling & Fischer, 1998). This is not practical for young children, but an analogous task is “counterpointing” (Atkinson et al., 2003) in which the child is required to follow the rule of pointing to the opposite side of the screen to that where the target appears. The specific difficulties of children with Williams syndrome with this task, compared to verbal inhibition tasks, are discussed below, and suggest that, at least in this neurodevelopmental disorder, visuo-spatial executive function can have distinct underpinnings from control of non-spatial (e.g., sequential or verbal) behavior.

Of course, all measures of visual attention, and in particular executive function measures, are affected by the emotional and motivational significance of the stimulus material. This is an area where social brain development and visual brain development interact, with neural circuits in prefrontal cortex combining information from cortical visual and parietal areas, with modulation from the amygdala and other reward networks. The influences that operate emotionally and motivationally have been called “hot EF” with influences operating in more neutral contexts labelled “cool EF” Performance on hot EF measures is generally found to mature later in the age range eight to fourteen years than for cool EF tasks (Carlson et al., 2013).

Development of Visuo-Spatial Localization and Spatial Memory

Vision serves to provide the information that identifies familiar locations in the environment, allowing navigation through that environment and tagging the location of significant properties that are not themselves visible (spatial memory). Adult and animal neuropsychology and brain imaging show that dorsal-stream parietal networks are the primary processing areas for basic spatial localization, while the hippocampus, parahippocampal gyrus, and entorhinal cortex are involved in more complex spatial memory tasks.

Tests of location memory can serve to identify the visual information used by children at different ages, and the spatial framework which they use to define the locations. Infants under one year use representations that are primarily egocentric (using the body as a reference), as shown in studies of their characteristic A-not-B place error (e.g., Bremner, 1994). However, they can identify an allocentric location (invariant as the child moves) defined by sufficiently prominent landmarks (Acredolo & Evans, 1980). Prefrontal, posterior parietal, and hippocampal maturation lead to improvements in spatial memory representations in mid-childhood (see Klingberg, 2006), using external landmarks to guide action and retrieve hidden objects as the child walks around at twelve to thirty six months (Huttenlocher, Newcombe, & Sandberg, 1994; Newcombe, Huttenlocher, Bullock Drummey, & Wiley, 1998). Nardini, Burgess, Breckenridge, and Atkinson (2006) showed that children had to be five years old before they could define a position from local landmark features whose position changed relative both to the body and to more distant (room) landmarks, an ability which in adults is thought to depend mainly on hippocampus circuitry (O’Keefe & Burgess, 1996).

Hippocampal representations of space depend heavily on the geometry of the environment, in particular relationships of locations to enclosing boundaries (O’Keefe & Burgess, 1996). Hermer and Spelke (1994, 1996) found that eighteen to twenty four month-olds, disoriented by being rotated within a rectangular enclosure, recalled the location of a hidden toy using the geometry of corners, but ignored information from the color of the walls. They argued for an early specialized geometric module, and that use of the color cue depended on development of linguistic labels (Hermer-Vazquez, Spelke, & Katsnelson, 1999). While there is evidence against both ideas (Nardini, Atkinson, & Burgess, 2008b), the early dominance of room geometry over color for spatial orientation remains a striking phenomenon which is also reflected in behavior in children less than two years of age on search tasks not involving disorientation (Nardini et al., 2008b). The “disregard of color” may be a common developmental phenomenon, reflecting poor integration of dorsal and ventral visual streams in these tasks which affects the salience of colors, relative to actions and spatial cues in guiding behavior.

Abnormalities and Plasticity of Visual Development

Advances in methods and findings on typical visual development allow us to characterize, and hopefully to remediate, the ways in which this development can go wrong. In turn, developmental disorders of vision provide a powerful source of information about the normal processes of development. Such information comes first, from the pattern of deficit in disorders, and secondly from the evidence they provide on how the developing brain adapts to abnormal visual input. It shows the long-term impact of disorders in infancy, but also the remarkable plasticity of the infant visual brain in ameliorating this impact.

Blindness and Visual Impairment

International definitions (e.g., World Health Organization, 2007) and criteria for registration as “blind” or “visually impaired” are expressed in terms of acuity and visual field loss. These terms are of limited usefulness for understanding functional visual loss in infants and young children. First, they do not reflect the norms of developing visual acuity. Secondly, in developed countries, childhood visual loss is most often related to abnormal development of the brain, with related functional visuo-cognitive deficits (“cerebral visual impairment,” discussed below).

Pathology within the eyes or optic nerve is the alternative cause of vision loss in childhood, for example, the retinopathy of prematurity linked to high oxygen levels in intensive care (Fielder, Blencowe, O’Connor, & Gilbert, 2015). This, and other ocular disorders, will not be considered further here except when they are causative factors for central abnormalities. Atkinson and Braddick (2008) provide a short review of both ocular and brain-related childhood visual disorders.

Binocularity and Strabismus

One of the commonest areas of visual developmental disorder is in the development of binocularity. Cortical connections combining information from the two eyes first become functional around three to five months of age, as discussed above. However, if the eyes do not maintain a precise motor alignment, signals from corresponding points of the two eyes do not provide correlated signals to the cortex, and binocular connections break down (Daw, 1995). Conversely, if the cortex cannot detect matches and mismatches of the two eyes’ images, it cannot control the fine motor adjustments that maintain convergence. It follows that there is a feedback loop maintaining binocular vision which is easily broken, either by a defect of neural transmission (as in the mis-routed optic nerve fibers found in albinism), or by a motor deficit such as weakness or paralysis of the eye muscles. This breakdown leads to misalignment of the eyes known as strabismus (or “squint” in the United Kindom), in which the failure of binocular cortical connections leads to the absence of stereoscopic depth perception. This vulnerable developmental feedback loop between eye movements and cortical connections may explain why strabismus is frequent in all kinds of neurodevelopmental disorders (Down’s syndrome, prematurity, perinatal brain injury, etc.) (see Sandfeld Nielsen, Skov, & Jensen, 2007).

Convergence of the eyes and accommodation (focusing) of the lens are closely linked. This may be why strabismus often occurs in hyperopic children, who have to accommodate to an abnormal degree. Atkinson et al. (2007) review their population screening programs of over 8.000 infants, which showed that infants who were hyperopic at age nine months were more likely to develop strabismus and/or amblyopia by four years, but that these problems could be reduced by spectacle correction in infancy.

Amblyopia and Plasticity

Amblyopia is identified as a loss of visual acuity due to anomalous visual experience, usually affecting one eye’s vision. It has no detected organic cause in the eye itself and cannot be improved with spectacle correction, but is believed to be a developmental disorder of neural connectivity in the visual cortex: strabismic amblyopia occurs when the two eyes’ signals are uncorrelated due to misalignment; anisometropic amblyopia when one eye’s image is blurred due to refractive error; and the most severe form, deprivation amblyopia, when an eye has no patterned input, most commonly due to cataract.

Animal models (Wiesel, 1982; Blakemore & van Sluyters, 1974), and clinical experience, indicate the existence of a critical period for establishing binocularity. If coordinated signals are not provided to the cortex before about three months of age in kittens, and probably about two to three years in human infants, binocular connections in the brain cannot easily be re-established even if the eyes are subsequently aligned surgically. For example, Banks, Aslin, and Letson (1975) showed that cortical binocularity, assessed by transfer of an after-effect between the eyes, was increasingly impaired if an infant’s strabismus was corrected later than age two years. Earlier strabismus surgery can be shown to re-establish binocularity (Smith, Atkinson, Anker, & Moore, 1991) although this binocularity is fragile, as evidenced by its decline in many of these children by four years of age.

So, these results suggest that neural connections in the cortex remain modifiable (or plastic) for a limited critical period. The development of amblyopia shows similar plasticity, although the period when it can be effectively corrected is the subject of controversy (Daw, 1998; Levi, Knill, & Bavelier, 2015). Neurobiological evidence (Hensch, 2005) suggests that the development of specific inhibitory circuits in the cortex plays a key role in regulating this period of plasticity.

For many years amblyopia has been treated by patching the non-amblyopic “fellow” eye in childhood, to force the amblyopic eye to be used for fixation and hopefully improve that eye’s neural connections to the cortex. The optimal regime for patching and its effectiveness at different ages remains controversial (Stewart, Moseley, & Fielder, 2011). Recent work has highlighted that monocular stimulation may not be the best approach to restoring binocular function. Promising new therapies require the individual to use their two eyes together, for example when each eye is presented with different elements of a video game (Levi et al., 2015; Hess & Thompson, 2015). These therapies reveal the potential for re-establishing binocularity even in adulthood.

Although amblyopia is usually clinically assessed in terms of visual acuity, the actual visual consequences of visual deprivation are considerably more complex. Amblyopic individuals lose not only the ability to detect fine detail, but also some of its spatial organization: patterns may appear “scrambled” and text is confused by “crowding” effects. Furthermore, although studies of neural plasticity have emphasized effects on the synapses where signals from each eye arrive at V1 neurons, there is a great deal of evidence of deficits at higher processing levels, for example in global motion processing (Simmers, Ledgeway, Hess, & McGraw, 2003; Simmers, Ledgeway, & Hess, 2005; review by Hamm, Black, Dai, & Thompson, 2014). These deficits can affect the fellow eye as well as the amblyopic eye (Giaschi, Regan, Kraft, & Hong, 1992; Hamm et al., 2014).

Thus early deprivation has far-reaching effects on the development of the visual system. These are seen most strikingly in people who had cataracts in one or both eyes at birth, which were surgically removed in the first year of life. These cases show persisting deficits in global motion processing, global form processing, and face recognition, which are not explained by any remaining effect on acuity (Maurer, Lewis, & Mondloch, 2005; Putzar, Hötting, Rösler, & Röder, 2007). They show that early visual deprivation can affect visual capabilities which have not yet emerged when vision is restored, indicating how experience is required to set up the infrastructure for later development in both the dorsal and ventral streams (Maurer, Mondloch, & Lewis, 2007). Unlike the amblyopic effect on acuity, these deficits are less severe for monocular than binocular deprivation. It is argued, therefore, that the plasticity at early levels involves synaptic competition between the two eyes, but that at a higher cortical level, “scaffolding” established by one eye’s input can aid later development of the deprived eye’s connections.

High-level effects are also seen in association with children who were hyperopic in infancy, beyond their increased rate of strabismus and amblyopia. These children show subtle delays in development of visual attention and in visuocognitive, visuomotor, and spatial abilities, first identifiable in the second year of life and persisting into the beginning school years (Atkinson et al., 2007). However, it is not clear whether their refractive errors have any casual role in these problems, or whether the persistence of hyperopia is a signature of impaired development in visuo-cognitive brain systems.

Long term deprivation of pattern vision can lead to radical and apparently permanent impairment of many aspects of visual function, as exemplified by a case who suffered a blinding accident at three years of age and subsequent surgical repair in middle age (Fine et al., 2003). However, a program of surgery repairing congenital cataracts in children in rural India (“Project Prakash”: Sinha, 2013) has shown initial deficits, but remarkable recovery of visual capabilities over a short period (Ostrovsky, Meyers, Ganesh, Mathur, & Sinha, 2009), including the understanding of visual-haptic correspondences (Held et al., 2011). The differences in outcome in these cases are not yet understood, and may depend on the residual visual experience received over a long period of apparent pattern deprivation.

Cerebral Visual Impairment

Although there remain many children who are blind or severely visually impaired due to pathology in the eyes (see Atkinson & Braddick, 2008, for an outline), the greatest cause of visual impairment in developed countries is “cerebral visual impairment” (CVI)—a severe deficit of visual behavior as a result of brain damage, usually occurring around birth and particularly in children born very prematurely. There are occasional cases described as “delayed visual maturation,” showing complete isolated visual inattentiveness in the first months of life, without identified neurological damage, but recovery of normal visual attentiveness by around six months of age (Mercuri et al., 1997d). This pattern suggests a delay in the onset of cortical and subcortical visual networks, for reasons that are not understood. Much more frequently, early lack of visual responses is associated with identified brain damage and is long-lasting.

Severe CVI is unlikely to be an isolated impairment. The underlying neurological damage often leads to cerebral palsy, developmental delay, and/or other impairments. More recently, following ideas on deficits related to dorsal and ventral streams (see sections above and below), CVI has been used to describe a whole range of visual impairments from mild to severe, including some visuo-cognitive impairments (e.g., Dutton, 2013).

Because cortical visual function develops early, visual measures in the first year of life can provide a sensitive signature of cerebral problems whose wider cognitive and motor effects is only detectable later. Earlier sections have described the measures of orientation-reversal VEP and fixation shifts: deficits in these and other visual indicators have been found in infants with perinatal focal lesions (Mercuri et al., 1996) or the more diffuse damage of HIE (hypoxic-ischemic encephalopathy) which results from oxygen deprivation around birth (Mercuri et al., 1997a, 1998), and in very prematurely born children (Atkinson et al., 2008). The damage in these cases is not necessarily to the classical visual areas of the cortex: Mercuri et al. (1997b) found that visual losses were most severe when the subcortical structures of the basal ganglia were damaged. There is a remarkable plasticity which can enable the transfer of visual functions from damaged to undamaged cortex in infancy (Tinelli et al., 2013) which may be absent in the basal ganglia—alternatively the basal ganglia or adjacent structures may play a key role in enabling this plasticity of visual cortical pathways.

The indicators of early cortical visual function are also predictors of later development beyond the purely visual domain; children showing these deficits in infancy, whether through HIE (Mercuri et al., 1999) or prematurity (Atkinson & Braddick, 2007; Atkinson et al., 2008) have a poorer outcome in cognitive assessments at two years and beyond.

Dorsal Stream Vulnerability

An earlier section introduced global form and motion sensitivity as indicators of the relative development of ventral and dorsal cortical streams. These were first used for investigating atypical development in the case of Williams syndrome (WS). WS is a chromosomal disorder with a characteristic pattern of developmental delay, showing severe impairment of visuospatial abilities alongside relatively good recognition and language abilities, a pattern which suggested a specific impairment of the dorsal stream. This idea was supported by finding a marked deficit in global motion compared to global form sensitivity (Atkinson et al., 1997), which persists into adulthood in WS (Atkinson et al., 2006). The same study also showed specific impairment of posting a card through an angled slot, a visuomotor skill which is known to reflect preserved dorsal stream function in neuropsychological patients (Milner & Goodale, 1995; Perenin & Vighetto, 1988), and neuroimaging studies also indicate possible dorsal stream anomalies in WS (Mercuri et al., 1997c; Meyer-Lindenberg et al., 2004).

However, many later studies indicated that the relative impairment of motion processing was not special to WS. Poor global motion sensitivity was found in autism (e.g., Spencer et al., 2000), perinatal brain damage resulting in hemiplegia (Gunn et al., 2002), prematurity (e.g., Atkinson & Braddick, 2007; Taylor, Jakobson, Maurer, & Lewis, 2009), children with Fragile X (Kogan et al., 2004), children with early congenital cataract (compare Ellemberg, Lewis, Maurer, Brar, & Brent (2002) with Lewis et al. (2002)) and in dyslexia (e.g., Hansen, Stein, Orde, Winter, & Talcott, 2001). This led Atkinson and Braddick to put forward the hypothesis of “dorsal stream vulnerability” (DSV), that is, the dorsal stream is specifically vulnerable in both genetic and acquired developmental disorders (for reviews see Braddick, Atkinson, & Wattam-Bell, 2003; Atkinson, 2017). The idea of DSV has been expanded beyond motion processing to include vulnerability in other areas (visuomotor control of actions in spatial cognition, visual attention including executive functions), where processing takes place in many interacting areas within dorsal stream networks. This idea is discussed in the following paragraphs below.

As outlined in earlier sections, the dorsal stream plays a key role in visuomotor control, spatial attention, and spatial cognition, and deficits in these visually related functions are found across many developmental disorders. WS individuals have problems in walking over uneven surfaces, stepping down from curbs, walking down stairs (Withers, 1996; Chapman, du Plessis, & Pober, 1996; Atkinson et al., 2001; Hocking, McGinley, Moss, Bradshaw , & Rinehart, 2010; Hocking, Rinehart, McGinley, Moss, & Bradshaw, 2011; Cowie, Braddick, & Atkinson, 2012); block construction copying and shape fitting tasks from the ABCDEFV (Atkinson et al., 2001); fine motor movements, ball skills, dynamic and static balance from the ABC Movement Battery (Henderson & Sugden, 1992; Atkinson et al., 2001; Atkinson, 2017); end-point comfort planning (Smyth & Mason, 1997; Newman, 2001; Braddick & Atkinson, 2013); deficits in location memory tasks in using allocentric frames of reference and in navigation tasks (e.g., Nardini, Atkinson, Braddick, & Burgess, 2008a; Mandolesi et al., 2009; Broadbent, Farran, & Tolmie, 2014; Farran, Formby, Daniyal, Holmes, & Van Herwegen, 2016). Visuomotor spatial problems also occur in children with significant hyperopia in infancy (Atkinson et al., 2002b, 2007); children born very prematurely (e.g., Atkinson & Braddick, 2007; de Kieviet, Piek, Aarnoudse-Moens, & Oosterlaan, 2009; O’Connor, Birch, & Spencer, 2009; Geldof, van Wassenaer, de Kieviet, Kok, & Oosterlaan, 2012; Birtles et al., 2012; Braddick & Atkinson, 2013; Bos, Van Braeckel, Hitzert, Tanis, & Roze, 2013); children with Autistic Spectrum Disorder (e.g., Fournier, Hass, Naik, Lodha, & Cauraugh, 2010; Whyatt & Craig, 2012; Liu, 2013; Simermeyer & Ketcham, 2015; Paquet, Olliac, Bouvard, Golse, & Vaivre-Douret, 2016; Purpura, Fulceri, Puglisi, Masoni, & Contaldo, 2016); dyslexia (e.g., Haslum & Miles, 2007); and amblyopia (e.g., Grant, Suttle, Melmoth, Conway, & Sloper, 2014).

Attention problems are similarly widespread across many developmental disorders (reviewed by Atkinson & Braddick, 2012). Fixation shift deficits in children with perinatal brain damage have been outlined above and by Hood and Atkinson (1990), and also occur in Williams syndrome (Atkinson et al., 2003). Older children born very prematurely show persistent deficits in a range of tests of attention, including executive function (Atkinson & Braddick, 2007; Mulder, Pitchford, Hagger, & Marlow, 2009). These tests also show deficits in Williams and Down’s syndromes beyond those expected for these children’s general mental ages, although the pattern is not identical across syndromes, with WS showing greatest impairment in counterpointing, an executive function task with specific spatial demands (Atkinson et al., 2003; Breckenridge et al., 2013b).

In contrast, specific developmental problems related to ventral stream function are relatively rare. “Prosopagnosia” is a specific deficit in face recognition, and a group of adults have been identified with “developmental prosopagnosia” without any other associated pathology (Susilo & Duchaine, 2013). However, so far it has only rarely been possible to show a childhood origin of this condition (Dalrymple, Corrow, Yonas, & Duchaine, 2012).

While the vulnerable areas of motion processing, visuomotor coordination, attention, and spatial cognition all have underpinnings in the dorsal stream, the links between them in atypical development are not yet understood. It is unknown whether any particular deficit is primary, leading to the others via a developmental cascade; whether the demands of temporal precision in motion and motor processing form a particular factor in their prolonged and vulnerable development; whether integration of dorsal and ventral streams is a critical factor; or whether the patterns of causality are similar in the very diverse conditions that show this vulnerability. Hopefully future longitudinal studies combining neural and behavioral measures may help to unpick these puzzles.

In the meantime, it is clear that research on the emergence of visual brain functions in typical development has helped to understand disorders of vision and visual cognition, and vice versa. It is to be hoped that future research unifying typical and atypical development, and clearly identifying the underlying developmental functional eye-brain networks and their relative vulnerabilities, may lead to further scientifically informed diagnosis and effective treatment, so that all children reach their full “visual” potential.


Much of the research discussed in this article was supported by awards from the U.K. Medical Research Council, with additional funding from the U.K. Economic & Social Research Council, the European Union, National Institutes of Health, Williams Syndrome Foundation, Wellcome Trust, and the Leverhulme Trust.

I thank all my colleagues and collaborators around the world, in particular the team of the Visual Development Unit, whose names appear as my co-authors in the cited references. But, primarily, I thank Oliver Braddick, without whose collaboration and support none of this would have been possible.


  • ABCDEFV = Atkinson Battery of Child Development for Examining Functional Vision.

    A standardized battery of tests for the zero to six year age range to assess how far a child is making effective use of vision. It includes core vision tests which are designed not to rely on the level of the child’s manual, verbal, or cognitive skills (e.g., diffuse light reaction, tracking, acuity measured using preferential looking, accommodation) and additional more advanced tests of perceptual, cognitive, and spatial vision which require reaching and grasping with at least one hand (e.g., retrieving covered object, shape matching, identifying embedded figures, copying block designs). Full details are given in Atkinson et al. (2002a).

  • Accommodation.

    Adjustment of the lens of the eye to bring objects at different distances into sharp focus on the retina.

  • Acuity.

    A measure of the finest detail that can be resolved. Often measured as the smallest letters that can be read (e.g., on the Snellen chart) and expressed in relation to the normative value. Alternatively, tested as the finest grating of black and white stripes that can be distinguished from a uniform field of the same average luminance. The Snellen chart and similar charts contain rows of successively smaller letters. Children of three to five years can more easily identify letters, or simply shaped symbols, when presented on individual cards as in the Lea Symbols test or the Cambridge Crowding Cards. Acuity may be expressed either as a fraction of “normal” adult acuity at six meters or 20 feet (e.g., 6/6 or 20/20), as a decimal fraction of “normal” adult acuity (e.g., 0.5) or, for grating acuity, as the highest spatial frequency that can be detected. Thus, the typical acuity of a three-month infant measured by preferential looking can be expressed as 6/60, 20/200, or 0.1, or 3 cycles/deg.

  • Amblyogenic.

    Describes a condition (e.g., strabismus or anisometropia) which may lead to amblyopia.

  • Ambylopia.

    A loss of visual acuity which cannot be explained by the optical effects of refractive error or by pathology of the eye. Rather, amblyopia is believed to result from functional changes in neural connections, primarily in the visual cortex, that result from degraded visual input. Amblyopia is most commonly a result of anisometropia or strabismus, which impair visual information coming from one eye compared to the other.

  • Anisometropia.

    A difference of refraction between the two eyes, for example where one eye has a significantly greater degree of hyperopia than the other. Often a cause of amblyopia.

  • Astigmatism.

    A difference in refraction of the eye between different meridians, usually caused by the cornea having different degrees of curvature in different directions. For example, when the lens is adjusted to focus on vertical contours at a particular distance, horizontal contours at that distance will be out of focus, and vice versa.

  • Basal ganglia.

    A set of large nuclei deep within the cerebral hemispheres, connected by loops to and from various areas of the cortex, and also with the thalamus and subcortical nuclei. Their best-established function is in the initiation and control of patterns of motor action, but they probably have a much wider function in transmitting and modulating cortical activity.

  • Binocular.

    Using the two eyes together.

  • Binocular disparity.

    Difference between position of images of an object as viewed by the two eyes. Binocular neurons in visual cortex detect these differences which underlie the perception of depth differences by stereopsis.

  • Cambridge Crowding Cards (CCC test).

    An acuity test suitable for children from three-and-a-half years upwards (and individuals with intellectual disabilities or communication difficulties), which is sensitive to the effects of crowding. The child is required to match a central letter which appears surrounded closely by four others on each card. The child does not need to know the names of the letters, or speak English. The size of the letters is progressively reduced over a series of cards The CCC test is a child- friendly substitute for an adult letter chart (such as the Snellen chart).

  • Cataract.

    An opacity in the lens of the eye. A severe cataract can completely abolish pattern vision through that eye. It is normally treated surgically by removal of the lens and fitting a contact lens or implant to restore normal refraction. After removal of a unilateral cataract, amblyopia may remain.

  • Cerebral cortex.

    See cortex.

  • Contrast sensitivity.

    The ability to detect the difference between light and dark parts of the image. It can be measured as the minimum contrast required to see gratings at different spatial frequencies, typically plotted as the contrast sensitivity function (CSF). Acuity is the spatial frequency on the CSF at 100% contrast, where the grating is just visible.

  • Convergence.

    See vergence.

  • Cornea.

    The curved transparent surface at the front of the eye, through which light passes into the pupil. The curvature of the cornea, along with that of the lens, is responsible for focusing light from distant objects onto the retina. Astigmatism in infants is often due to the curvature of the cornea.

  • Cortex.

    The outermost part of the hemispheres of the brain, made up of layers of interconnected cell bodies of neurons and believed to be the major site of the computational operations underlying perception, cognition, and decision making.

  • Crowding.

    The reduction of acuity when a test item (e.g., letter) is surrounded closely by other letters or other contours, compared to acuity of an isolated letter. It is particularly marked in young children and in amblyopia. It means that the level of visual impairment may not be adequately assessed by testing acuity with isolated letters or grating patterns. See Cambridge Crowding Cards.

  • Dorsal stream.

    A series of cortical areas, transmitting visual information from V1 through the parietal lobe of the brain, which includes areas specialized for motion and extracts information that provides a sense of spatial relationships, the basis for visually guided actions, and is strongly related to spatial attention.

  • EEG = Electroencephalogram.

    A recording, from electrodes attached to the surface of the head (often secured by a net or cap), of mass electrical activity within the brain. VEPs or visual evoked potentials (often called “VERPs –visual event related potentials”) are a component of the EEG that can be specifically related to the occurrence of a visual stimulus event.

  • Emmetropia.

    The ideal refractive condition in which, when accommodation is relaxed, very distant objects are sharply focused on the retina, and thus varying degrees of accommodation can adjust focus for the range of distances down to the near point.

  • Emmetropization.

    The development of refraction during childhood in the direction of emmetropia (most commonly from an initially hyperopic refraction). There appear to be active mechanisms which respond to the level of habitual defocus of the eyes and control the growth of the eye so that emmetropization tends to occur.

  • Evoked potentials.

    See VEP.

  • Extrastriate cortex.

    The collection of visually responsive areas of cortex which surround area V1 and receive input from it directly or indirectly. It includes areas V2, V3, V3a, V4, and V5 (often called “MT”) and LO (=lateral occipital).

  • FEF = frontal eye fields.

    A region of the frontal cortex, in front of the motor cortex, which is involved in the control of eye movements. It sends signals directly and indirectly to the superior colliculus.

  • Fixation.

    The act of moving the eye, or maintaining its direction, so that the object of interest is focused on the fovea. Sometimes called “fixing” in newborns.

  • fMRI.

    See MRI.

  • Focal lesion.

    A lesion that is localized in a particular region of the brain, for instance due to a hemorrhage at that location, usually identified in brain imaging (MRI).

  • Form coherence (global form).

    A measure of the global visual processing that integrates information about static shape and pattern in the ventral cortical stream. It is tested by an observer’s ability to detect in an array of short line elements that some percentage of the elements (the percent coherence) are arranged in a specific pattern, for example concentric circles, the remaining elements being randomly oriented. Compare motion coherence.

  • Fovea.

    The region in the center of the retina where the cone photoreceptors are most densely packed, and which therefore provides the highest acuity and is normally used to fixate the object of interest.

  • FPL.

    See preferential looking.

  • Fusiform gyrus.

    A region on the ventral surface of the brain between the occipital and temporal lobes which forms part of the ventral stream. It includes the fusiform face area (FFA) which in fMRI tests is more strongly activated when the subject is viewing faces than for any other stimuli. It is therefore presumed to be one of several specialized areas for processing the visual information used to detect and recognize faces.

  • Global visual processing.

    Visual processing that involves combining information over an extended region of the field of view, to recognize its large-scale structure (see form coherence and motion coherence) Global processing takes place in extrastriate regions, in contrast to the more local visual processing performed in area V1.

  • Grating.

    See spatial frequency.

  • Habituation/recovery.

    A method of investigating the ability of young infants to distinguish different visual patterns. If one pattern is presented repeatedly, the time spent by the infant looking at it declines (habituation). If the looking time increases when a new pattern is presented (recovery), this is evidence that the infants can distinguish the two patterns and so respond to the novelty of the new pattern.

  • Hemispherectomy.

    A surgical operation to remove all or most of one of the cerebral hemispheres, while leaving subcortical structures intact. It is usually carried out in young children to relieve intractable epileptic seizures caused by congenital malformation of one hemisphere, when treatment with antiepileptic drugs has proved ineffective.

  • HIE = hypoxic-ischemic encephalopathy.

    Widespread brain damage caused by a general deprivation of oxygen (hypoxia), often due to a reduction of blood flow (ischemia). Sometimes a consequence of reduced oxygen and/or blood supply during the events of birth. This damage is diffusely spread throughout the brain, in contrast to a focal lesion.

  • Hyperopia or hypermetropia.

    State of refraction in which, when accommodation is relaxed, the curvature of the cornea is insufficient to bring the light from a distant object into focus on the retina. The relaxed eye is focused “beyond optical infinity.” At each closer distance, a greater degree of accommodation is required, compared to an emmetropic eye, to focus on the object. Sometimes known as “long-” or “far-sightedness.”

  • LGN = lateral geniculate nucleus.

    A nucleus in the thalamus where the fibers of the optic nerve terminate. Axons of neurons in the LGN form the optic radiation. Thus, the LGN is the intermediate way-station between the retina and visual cortex.

  • LO = lateral occipital.

    An area on the lateral and ventral aspects of the human occipital cortex, which is found in fMRI tests (on adult) as strong activation to intact images of objects and scenes as opposed to scrambled versions of the same images. As such it is believed to be an important component of the ventral stream, transmitting the information required for object recognition.

  • Local visual processing.

    Operations which extract visual information from a small region of the image, for example the orientation of a short length of contour which is signaled when the contour segment falls on the small receptive field of a neuron in area V1. (see Global visual processing).

  • Monocular.

    Relating to one eye only (contrast with binocular). For example, Monocular depth cues in contrast to stereopsis (Both eyes viewing).

  • Motion coherence.

    A measure of the global visual processing that integrates information about motion in the dorsal cortical stream. It is tested by an observer’s ability to detect in an array of moving dots when some percentage of the dots (the percent coherence) are moving in a consistent direction, although the remaining dots are moving in random directions.

  • MRI = magnetic resonance imaging.

    A technique which uses the reaction of hydrogen nuclei to strong magnetic fields, to provide a high-resolution image of the brain. The commonest application is to give a structural image in which grey matter, white matter, and fluid are clearly distinct. Functional MRI, or fMRI, uses the distinct magnetic properties of oxygenated blood to detect which locations in the brain are demanding oxygen, a correlate of local neural activity. Structural MRI is used for neurological investigation at all ages, but fMRI requires a conscious individual to maintain a motionless position in the scanner, and so is very difficult with very young children.

  • MT = middle temporal.

    An alternative name for the cortical visual processing area V5, which is specialized for visual motion processing. In human brains it is located near the temporal/occipital/parietal junction.

  • Myelination.

    Development of the myelin sheath which improves rapid conduction along nerve fibers. Myelination of the optic nerve develops over the first two years; myelination of white matter tracts connecting cortical areas continues well into adolescence.

  • Myopia.

    State of refraction in which, even when accommodation is relaxed, the curvature of the cornea is such that light from objects at some near distance (e.g., 20 cm, is brought to focus on the retina. Sharp images cannot be achieved for more distant objects. Sometimes known as “short-” or “near-sightedness.”

  • NIRS = Near infra-red spectroscopy.

    A technique for measuring and localizing brain activity through associated changes in oxygenated and de-oxygenated blood (a similar measurement to that in functional MRI). The method measures the absorption at specific wavelengths of infra-red light from an array of sources on the scalp; the light shines through the skull and brain tissue. As the sources and detectors are attached to the head, it is less disrupted by the child’s head movement (but also much lower spatial resolution) than fMRI.

  • Nystagmus.

    Repetitive oscillatory movements of the eyes. This may be due to an imbalance of the oculomotor system, to an inability to register a target for fixation due to total or partial blindness, or may be induced by a stimulus (see OKN).

  • OKN = optokinetic nystagmus.

    Nystagmus induced by motion of all, or a large part of, the field of view, as when looking out of the side window of a moving train or bus. The eyes repetitively follow the movement of the field and then flick rapidly back with a saccade-like motion in the opposite direction. This reflex response acts to stabilize the image on the retina.

  • Optic nerve.

    The bundle of nerve fibrer which originate as axons of retinal ganglion cells and which convey visual information from the eye to the brain. The later part of this fiber bundle is named the optic tract. The fibers terminate in the lateral geniculate nucleus (LGN) of the thalamus.

  • Optic radiation.

    The fiber tract which carries visual information from the LGN to area V1 of visual cortex. It forms the majority of the white matter in the occipital pole of the brain.

  • Photoreceptors.

    The sensitive cells within the retina which convert light energy into electrical signals that can be processed by other nerve cells in the retina and brain. Rod photoreceptors are very sensitive to dim light but do not provide good acuity or color vision. The cone receptors, less numerous than rods except in the fovea, provide high acuity and can signal the difference between different wavelengths (colors) of light.

  • Photorefraction.

    A method of estimating the refractive state of the eye, by recording photographically the pattern of light returning through the pupil of the eye from a small, safe flash source aligned with the camera lens. The method of isotropic photo or video refraction has the advantages that it does not depend on bringing lenses close to the infant or child’s eyes, and that it only requires very brief attention for the flash image to be captured. It can be used at any age, and is particularly appropriate testing refraction in very young infants and in children with developmental delay, including rapid mass vision screening programs to detect amblyogenic conditions. However, exact measurement for spectacle prescription, especially of large refractive errors, may still require the more difficult clinical method of retinoscopy.

  • PPA = parahippocampal place area.

    A region of the temporal lobe of the cerebral cortex, closely adjacent to the hippocampus. fMRI tests show that it is most active when viewing scenes such as the interior and exterior of buildings, especially for familiar locations. It has been proposed that the PPA extracts information about visually identifiable locations, required by the hippocampus for its functions of spatial memory and navigation.

  • PPC = Posterior parietal cortex.

    A complex of brain areas which receive information from extrastriate visual areas and forms part of the dorsal stream. The PPC is believed to be involved in transforming visual spatial information into the representations required for control of various types of visually guided actions. For example, specific distinct areas have appropriate properties for visually controlling reaching, grasping, and saccadic eye movements.

  • Preferential looking.

    A method of testing infant vision by measuring the infant’s preference for looking at a patterned screen compared with a blank one of matched mean contrast. By finding the highest spatial frequency of a grating pattern for which the infant shows a preference, the infant’s acuity can be estimated. Forced-choice preferential looking (FPL) requires an observer to choose which side the infant prefers to look, without knowing on which side the pattern has been presented. This is a simple, but efficient and objective, method of using the information conveyed by the infant’s looking behavior. However, if the child has a marked attentional loss, or poor eye movement control, the acuity assessment from FPL may be an underestimate of the child’s acuity.

  • Pulvinar.

    A group of nuclei in the thalamus, which provide a second route (besides the LGN) for visual information to reach the cerebral cortex. It is widely believed to play an important role in the attentional regulation of sensory processing.

  • Receptive field.

    The region of the field of view within which stimuli can excite or inhibit the response of a particular neuron in the visual system.

  • Refraction.

    The process of measuring the distance at which an eye is focused; also the result of this examination, in terms of the degree of hyperopia, myopia, and/or astigmatism present in the eye. The normal aim of clinical refraction is to measure the focus of the eye when accommodation is completely relaxed.

  • Retina.

    The neural network, with supporting tissues and blood vessels, which covers the inside of the back of the eyeball. It includes the rod and cone photoreceptor cells and several types of nerve cell which transmit signals from them, including the retinal ganglion cells which convey visual information to the brain.

  • Saccades or saccadic eye movements.

    Rapid jerky movements of the eyes which are used to move fixation from one object to another in the field of view.

  • Smooth pursuit.

    A form of eye movement which matches the velocity of the eye to that of a moving target, and so maintains the image of the target on the fovea. Pursuit can only be elicited by a stimulus in motion; otherwise any attempt to move the point of fixation is executed as a saccadic eye movement.

  • Spatial frequency.

    A measure of the scale of detail present in a pattern. For a grating pattern of parallel black and white stripes, the spatial frequency is measured as the number of cycles (paired black and white stripes) within one degree of visual angle. Thus, the limit of normal adult visual acuity can be expressed as 30–40 cycles/degree. Any scene or pattern also contains lower spatial frequencies which represent the coarser distribution of light and dark in the image.

  • Stereopsis or stereoscopic vision.

    The ability to use binocular disparities present in the pair of images in the two eyes, to perceive the relative distance and three-dimensional modelling of objects in the scene. It depends on nerve cells in visual cortex receiving and processing signals from the two eyes together, and can be impaired or abolished when strabismus prevents this from occurring.

  • Strabismus.

    A condition where the axes of the two eyes are misaligned and so look in different directions, often called “squint.” One eye may be turned inward relative to the other (convergent strabismus or esotropia, sometimes known as “cross-eyes”); if one eye deviates outwards it is divergent strabismus or exotropia. Strabismus prevents signals from images of a given object in the two eyes from coming together correctly in the visual cortex, and so interferes with the development of stereopsis. In addition, the deviating eye may lose functional connections in the brain and become amblyopic.

  • Striate cortex.

    An alternative name for area V1, named from the “Stripe of Gennari” where the fibers of the optic radiation terminate.

  • Superior colliculus.

    A structure in the midbrain, also known as the optic tectum, which receives input from the retina by a branch of the optic nerve. It sends output to oculomotor nuclei for the control of eye movements, and so is believed to be responsible for orienting behaviour in newborn infants whose cortex is immature.

  • Sweep VEP.

    A method for using steady-state VEPs to estimate the visual acuity of infants. The infant views a grating stimulus whose spatial frequency is progressively reduced. The VEP evoked by the stimulus consequently reduces in amplitude; the level of spatial frequency for which the amplitude reduces to zero is taken as a measure of the child’s acuity

  • Thalamus.

    A group of nuclei in the brain which receive inputs from various sense organs and relays them to the cerebral cortex (and also receives signals from the cortex which can modulate this transmission). The LGN provides the main thalamic relay for visual information to striate cortex; the pulvinar is another thalamic nucleus involved in vision.

  • V1 = striate cortex.

    The primary receiving area in the occipital lobe of the brain for visual information. Nerve cells in area V1 carry out initial local processing of orientation, motion and binocular disparity, and pass the results of the processing to extrastriate areas.

  • V2, V3, V3a, V4, V5.

    Extrastriate visual areas of the brain. Each area lays out a distinct map of the field of view and contains nerve cells specialized to analyze a particular aspect of the scene. In particular, area V4 contains cells which respond to pattern properties and to color, and is considered a stage within the ventral processing stream, while V5 and V3a respond strongly to the motion within a pattern and are considered part of the dorsal stream. Cells in these areas have larger receptive fields that in V1 and V2 and so are suited to carrying out more global processing.

  • Ventral stream.

    A series of cortical areas, transmitting visual information from V1 to the temporal lobe of the brain, which extracts information that enables the visual recognition of faces, objects, and scenes.

  • VEP/VERP = visual evoked potentials or visual event-related potentials.

    Electrical signals recorded non-invasively from the surface of the head, which arise from visual processing events in the underlying brain structures. The recording is synchronized with a repetitive stimulus, so that neural signals time-locked to visual events can be distinguished from background noise. Different events, for example flashes of light, reversals of black/white contrast, or changes of orientation, can be used to elicit responses related to different kinds of visual brain processing. Recordings may either be “transient,” in which the sequence of electrical brain events over at least one second is complete before the next visual stimulus arrives, or “steady state,” where successive visual events are repeated at a high rate such as eight per second, and the brain’s periodic response at this repetition frequency is measured.

  • Vergence.

    An eye movement which alters the relative direction of the two eyes. In a convergence movement, the eyes point further inwards, as when fixating a near object. A divergence movement is in the opposite direction.

  • Vernier acuity.

    The ability to make fine visual comparisons of position, for example whether two vertical lines are aligned or misaligned. The finest degree of misalignment which can be detected is considerably smaller than the smallest feature which can be resolved in simple visual acuity for gratings or letters. However, in amblyopia, and early in development, vernier acuity is generally worse affected than simple acuity.

  • Videorefraction.

    A version of photorefraction in which the pattern of light returning from the eye is captured by a video camera and so can be inspected, analyzed, and immediately interpreted, by feeding the video data to a computer.

  • Visual acuity.

    See acuity.

  • Visual cortex.

    The region in the occipital lobe of the brain which carries out at least the early stages of processing of the visual image. It includes the primary visual cortex (V1 or striate cortex) where incoming visual signals arrive from the eyes, and the extrastriate areas V2, V3, V3a, V4, and V5, which carry out further processing. Neural signals are passed to systems which integrate information with other senses, initiate and guide actions, match information to stored information in memory, and register the individual’s location in the environment; the distinction between “visual” areas and those engaged in these “motor” and “cognitive” functions are not clear cut.

Further Reading

Selected key references are marked with *** in the list below. The following are additional suggestions for further reading:

Arterberry, M. E., & Kellman, P. J. (2016). Development of perception in infancy: The cradle of knowledge revisited. New York: Oxford University Press.Find this resource:

Atkinson, J., & Braddick, O. (2008). Vision disorders and visual impairment. In M. Haith & J. Benson (Eds.), Encyclopaedia of infant and early childhood development (pp. 381–394). Oxford: Elsevier.Find this resource:

Atkinson, J., & Braddick, O. (2012). Visual attention in the first years: Typical development and developmental disorders. Developmental Medicine & Child Neurology, 54(7), 589–595.Find this resource:

Braddick, O., & Atkinson, J. (2011). Development of human visual function. Vision Research, 51, 1588–1609.Find this resource:


Acredolo, L. P., & Evans, D. (1980). Developmental changes in the effects of landmarks on infant spatial behaviour. Developmental Psychology, 16, 312–318.Find this resource:

Adams, D. W., & McBrien, N. A. (1992). Prevalence of myopia and myopic progression in a population of clinical microscopists. Optometry and Vision Science Journal, 69, 467–473.Find this resource:

Adolph, K. E., & Franchak, J. M. (2017). The development of motor behavior. Wiley Interdisciplinary Reviews: Cognitive Science, 8(1–2).Find this resource:

Ajina, S., & Bridge, H. (2016). Blindsight and unconscious vision: What they teach us about the human visual system. The Neuroscientist. Advance online publication.Find this resource:

Arterberry, M. E., Craton, L., & Yonas, A. (1993). Infants’ sensitivity to motion-carried information for depth and object properties. In C. Granrud (Ed.), Visual perception and cognition in infancy. Hillsdale, NJ: Lawrence Erlbaum.Find this resource:

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