Development of Vision in Infancy

Preferential looking

Infants’ spontaneous visual fixation is attracted to certain stimuli more readily than to others. In particular, infants prefer to look at patterned stimuli rather than regions of uniform brightness. This spontaneous behavior has served as the basis for a quantitative measure of stimulus visibility known as forced-choice preferential looking (FPL). In the FPL task, the infant is confronted with a randomized series of patterns of varying visibility, presented either on the left or the right of a test screen. An observer judges whether the infant's fixation behavior is biased to the left or the right on a trial-by-trial basis. If the observer's judgments agree (or disagree) systematically with the actual position of the stimulus, it can be said that the infant's behavior is under the control of the stimulus. Distributions of the observer's judgments for a series of stimulus values are used to plot a psychometric function that relates the observer's percent correct to the stimulus values presented to the infant. Thresholds are estimated by curve fitting and interpolation to a criterion value of percent correct.

Visual evoked potentials

Visual evoked potentials (VEPs) are electrical brain responses that are triggered by the presentation of a visual stimulus. VEPs are distinguished from the spontaneous electroencephalogram (EEG) due to their consistent time of occurrence after the presentation of the stimulus (time-locking). For example, the abrupt contrast reversal of a checkerboard pattern consistently produces a positive potential at the surface of the scalp at a latency of approximately 100 msec in adults. Time-locked responses to abrupt presentations are referred to as transient VEPs . A second method of recording VEPs, the steady-state method, uses temporally periodic stimuli. For commonly used pattern reversal stimuli, the frequency of the repetition is often specified as the pattern reversal rate in reversals per sec. This rate is twice the stimulus fundamental frequency (in Hz), which is more commonly used to describe the temporal frequency of pattern onset–offset stimuli. As the stimulus repetition rate increases, the responses to successive stimuli begin to overlap. At high stimulation rates, the response is comprised of only a small number of components that occur at exact integer multiples of the stimulus frequency. Activity at each of the frequency components of the steady-state response is characterized by its amplitude and phase, where phase represents the temporal delay between the stimulus and the evoked response.

The surface-recorded VEP reflects the activity of cortical visual areas, with contributions from subcortical generators being apparent only under highly specialized recording conditions. The primary adaptations of adult VEP recording techniques for infants involve the control of fixation through the use of fixation toys or super-imposed video images and the rejection of trials when the infant's fixation was not centered on the stimulus.

Ocular following movements

Both infants and adults make reflexive eye movements following the presentation of a moving target. Optokinetic nystagmus (OKN) is characterized by a repetitive saw-tooth waveform. Rapid displacement of large fields also elicits short latency ocular following movements. Ocular following can also take the form of slower, pursuit-like movements. Reflexive eye movements are controlled by a combination of cortical and subcortical mechanisms. Infrared tracking, electro-oculography, and naked-eye observation of the preponderant direction of eye motion (DEM) are the primary assays used in infants and pre-verbal children.

Hierarchy of visual processing

Figure 38.1 presents the schematic framework of visual processing that is used to focus the discussion of empirical studies of visual function in infants and young children. The visual processing hierarchy is divided into three stages: early, middle, and late. The progression from early to late correlates roughly with an ascent from the retina to the cortex and with a functional hierarchy corresponding to the complexity of the information extracted at each level. In this view, early vision begins in the retina and continues through the lateral geniculate and on into primary visual cortex. By the level of primary visual cortex, stimulus attributes such as orientation, direction of motion, and disparity have been extracted from the retinal images. Middle vision – the process by which local measurements of image features such as line orientation are integrated across space – begins no sooner than primary visual cortex and no doubt extends through a number of first- and second-tier extrastriate visual areas. The content of the representation at the level of middle vision includes information regarding the shape of extended contours, figure/ground relationships, the symmetry of objects, surface depths, but not the identity of the objects in the scene. The identification of objects (object recognition), which involves not only visual perception, but memory, is conceptualized as occurring in higher-order visual and visual association areas functionally associated with “late vision”.

Each of the different methods for assessing visual function in the pre-verbal child has a different relationship to the visual processing hierarchy. The FPL technique depends on the integrity of the early visual system as well as additional mechanisms responsible for the spontaneous preference for pattern (labeled “preference generator” in Figure 38.1 ). Whether or not middle or late mechanisms are invoked may depend on the discrimination the infant is called on to perform. Orienting behaviors could be driven from many levels of the cortical hierarchy or from subcortical structures. In any case, the output of the preference generator must produce robust fixation behavior that can be detected reliably by the FPL observer. Information regarding the location of the stimulus can be lost at the level of early vision, or at the level of the preference generator or by the observer of the infant's behavior. Given the additional sites for potential information loss after early vision, FPL is a conservative estimator of the function of the early part of the visual pathway.

Like FPL, the VEP depends on the integrity of the retina and an unknown amount of cortical processing. Fixation, in the sense that the stimulus must fall on central retina is required, but spontaneous orientation to a preferred stimulus is not. Electrical activity in the visual pathway is obscured by non-stimulus-related electrical activity associated with the EEG and muscle activity, as well as electrode-motion artifacts. The obscuring experimental noise can be reduced effectively, either through time-locked averaging or spectral analysis. At this point relatively little is known about the contribution of extrastriate cortical areas to the VEP. Given this, the VEP is quite likely to reflect the capabilities of early vision, but caution must be used in inferring the integrity of later stages of processing – especially if simple stimuli are used.

Ocular following movements require the integrity of the retina, certainly, but given the substantial role of subcortical mechanisms in the control of eye movements, it is difficult to specifically relate eye movement data to the hierarchy of cortical mechanisms in Figure 38.1 .

This review emphasizes developmental studies that have used the VEP. The rationale for this choice is several-fold. First, there is now sufficient evidence to indicate that the infant VEP is generated distal to the site of orientation selectivity, direction selectivity, Vernier offset detection, and binocular correlation detection. All these features are considered to be the outputs of early vision. In adults, it has been found that the VEP reflects both rivalry and suppression as well as several aspects of middle vision, including figure-ground segmentation based on either texture or motion. Second, the VEP does not require visual preference or transfer of information through the observation of spontaneous behavior and is thus less likely to underestimate the capabilities of early vision. Third, the VEP provides a rich source of information regarding the temporal dynamics of the visual response. Finally, there are already excellent reviews that have emphasized FPL and OKN measures of developing visual function. In deciding which studies to include, emphasis has been placed on those results that have been replicated by more than one research group, wherever possible. Data from the other methods are selectively discussed when these data can help to fill in gaps or when they illustrate particularly sharp contrasts.

Spatio-temporal vision

The retinal images contain a precise spatio-temporal mapping of the visual scene onto two-dimensional surfaces. At the most basic level of processing, the visual system must extract the contrast of the retinal images as a function of time and spatial scale. Visual sensitivity is limited by both spatial and temporal factors. Infant developmental studies have tended to focus on sensitivity along one dimension at a time – by measuring contrast sensitivity as a function of spatial frequencies for a fixed temporal frequency or vice versa. Sensitivity depends strongly on both parameters. While the FPL technique can be used at any combination of spatio-temporal frequencies, the eye movement and VEP measures each require temporally modulated stimuli. Given the fundamental importance of contrast sensitivity for subsequent visual processing, contrast sensitivity and the related function, grating acuity are among the few visual functions to have been studied extensively with each of the major methods discussed above.

Figure 38.2 plots peak contrast sensitivity as a function of age as determined by the steady-state VEP, directional eye movements, and FPL methods. Each of these studies obtained peak sensitivity measures at a mid-range of temporal frequencies (around 5–10 Hz). There is considerable development of contrast sensitivity in each of the techniques, but the absolute contrast sensitivity is higher with the VEP. By 10 weeks of age, infant peak contrast sensitivity over the 0.25–1 cycle per degree (cpd) range is within about a factor of 2–4 of adult levels measured on the same apparatus. Skoczenski & Norcia found a factor of 4 difference between infant and adult sensitivities at 1 cpd. Shannon and co-workers found sensitivities at 1.2 cpd that were a factor of 11 lower than adults at 2 months, with the difference decreasing to a factor of 4 at 3 months. Contrast sensitivity measured with the steady-state reversal VEP develops over progressively longer intervals as spatial frequency increases ( Fig. 38.3 ).

In contrast to the VEP, several behavioral measurements of contrast sensitivity in this age range are much lower than adult levels. Rasengane and colleagues reported that low spatial frequency flicker sensitivity of 2-month-olds was a factor of 45 lower than adults, with 3- and 4-month-olds being a little less than 20 times less sensitive with FPL. Brown and colleagues used a directional eye movement measure (0.31 cpd/ 15.5 deg/sec drift) and found that 3-month-olds were a factor of 100 less sensitive than adults on the same measure. Dobkins & Teller measured both FPL and directional eye movement thresholds in 3-month-olds. They found that infants were almost 30 times less sensitive on the directional eye movement measure and about 60 times less sensitive when FPL and adults' forced choice thresholds were compared. FPL and directional eye movement thresholds were within 20% of each other in the infants. In adults DEM thresholds were higher than psychophysical thresholds by a factor of 2–3, depending on whether the subject's task was detection of the direction of motion or simple contrast detection.

Hainline & Abramov used directional eye movements recorded by an infrared eye tracker to measure contrast sensitivity. The observer made a forced choice judgment on the output of the tracker (noise level 0.5 deg) rather than on naked eye observation. Contrast sensitivity with this method develops to adult levels by 5 months of age (see Fig. 38.2 ). Absolute thresholds are lower than those measured with the VEP by a factor of about 4. Hainline & Abramov's contrast sensitivities are higher than those observed by Dobkins & Teller or Brown and colleagues who used naked eye observation at substantially higher luminances. The difference in sensitivities obtained with naked eye and instrumented observation of eye movements suggests that at least some of the lower sensitivity seen in previous behavioral studies may have been due to information loss in the observer who is judging the infants' behavioral output.