Parallel Processes in Human Visual Development

Applications of Parallel hocessing in Vision J. Brannan (Editor) 0 1992 Elsevier Science Publishers B.V. All rights reserved

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Parallel Processes in Human Visual Development ADFUANA FIORENTINI

Introduction It has long been known that the human visual system is largely immature at birth, but until some twenty years ago not much was known about the visual functional properties of the newborn. or about the rate at which the visual system develops in the early period of infant life. The introduction of behavioral and electrophysiological techniques that could successfully be applied to study infant visual capacities has considerably increased our knowledge of the visual improvement that occurs after birth. A number of papers have appeared that review recent achievements in this field (for instance Aslin, 1987; Atkinson and Braddick. in press: Banks and Dannemiller, 1987; Gwiazda et al., 1989a; Teller and Bornstein. 1987). Only recently, however. it has become apparent that the time course of visual development may be quite different for different aspects of vision, even during the first year of life. This fact may reflect the different rates of maturation of classes of neurons which process in parallel various aspects of visual information. Unfortunately it is often impossible to assign the result of a human developmental study, either psychophysical or electrophysiological, to the maturation of a specific neural structure. In addition one has to take into account that visual development occurs both serially, a t various peripheral and central levels, and in parallel for various visual functions. In some cases the factors that limit infant vision are imposed in the eye by the physical and anatomical properties of the photoreceptors. b u t further constraints derive from immaturities of the neural structures in the retina and/or in the brain. In this chapter some recent findings are reviewed which provide the opportunity to speculate about the development of parallel neural pathways in the human visual system both a t peripheral and at central levels. Some inferences will be made regarding the possible contribution of the two major neural streams of the primate visual system, the parvocellular (P) and magnocellular (MIpathways, to some properties of infant vision and of its improvement in the early life period.

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Structural development The infant visual system undergoes profound structural changes in the early postnatal period. Some developmental modification continues during childhood (see Hickey and Peduzzi, 1987,for a recent review). Apart from an obvious increase in the size of the eyeball, there is in the retina a long maturation process, mainly in the macular region (Yuodelis and Hendrickson. 1986). The cones increase dramatically in length after birth and become increasingly thinner and more closely packed in the very center of the macula. At the same time the ganglion cells, a t birth still present in front of the receptors even in the center of the retina, migrate to occupy more eccentric positions allowing the foveal pit to take its adult shape. This process takes a few years to complete. Similar modifications have been reported to occur in the retina of macaque monkeys (Hendrickson and Kupfer, 1976). The optic nerve fibers, almost completely unmyelinated a t birth, acquire a myelin sheet that increases progressively in width. This process proceeds from the orbital portion of the nerve towards the eye. Almost all fibers are myelinated by 7 months of age, but the width of the myelin sheet continues to increase thereafter, especially during the first two years of life (Magoon and Robb, 1981). The Lateral Geniculate Nucleus (LGN)is structurally adultlike at birth, clearly differentiated into six layers, with two magnocellular ventral layers and four parvocellular dorsal layers (Hickey and Guillery, 1979). The cell bodies of the newborn are considerably smaller than those of the adult, both in the ventral and dorsal layers, and about two years are required to complete the process of cell body growth in the human LGN (Hickey, 1977). The rate of maturation is different in the parvo and magnocellular layers: while cells in the parvocellular layers (P cells) approach adult size by the end of the sixth month post term. those of the magnocellular layers (M cells) do not reach a comparable development until the end of the first year. However, the dendritic morphology of LGN cells seems to be mature by the end of the ninth month, both in the parvo and magnocellular layers (Garey and de Courten. 1983). Not much is known about the structural development of the human visual cortex in infancy. Synaptic density increases considerably from around two months after term till around eight months, when it reaches its maximum. Thereafter the number of synapses decreases. to stabilize at about eleven years (Garey and de Courten, 1983). A postnatal growth of dendritic branching has been described in layers 3 and 5 of the striate cortex, with layer 5 neurons maturing earlier (within 5 months from birth) than layer 3 neurons (Becker et al.. 1984). The latter take about two years to complete maturation. There is also some evidence that intracortical horizontal connections between columns develop mainly after birth (Burkhalter and Bernardo. 1989). One of the more important modifications functionally, which is known to occur in the striate cortex of infant monkeys, is the segregation of monocular LGN inputs to layer 4C. underlying the formation of ocular dominance columns. At birth the inputs from the two eyes overlap extensively in layer 4C while in the adult macaque

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monkey there is almost complete segregation (Hubel et al., 1977). Ocular dominance columns are known to be present in the human visual cortex, where they form a pattern similar to the monkey, although the single columns are considerably wider in the human adult than in the macaque (Horton and Hedley-Whyte, 1984). There is some evidence that ocular dominance columns in the human cortex form during the first six months of life. The columns have been found to be well formed in the cortex of 6 month old infants, but only poorly defined in the brain of a 4 month old infant (Hickey and Peduzzi, 1987: Horton and Hedley-Whyte, 1984).

Spatial characteristics: central vision The spatial characteristics of the adult visual system are best described by the contrast sensitivity function (CSF). which relates contrast sensitivity, Le., the reciprocal of the contrast threshold for resolving sinusoidal gratings, to stimulus spatial frequency (Campbell and Robson. 1968). Contrast thresholds can b e evaluated psychophysically or can be extrapolated from visual evoked potentials WEP) (Campbell and Maffei. 1970). A

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Figure 1. A Contrast sensitivity functions obtained from VEP responses to contrast-reversed sinusoidal gratings in one infant at three ages (in months) and in one adult subject (from Pirchio et al.. 1978). Mean luminance: 7 cd/m2; square-wave contrast reversal: 8 Hz. B: Average contrast sensitivity curves of infants of different ages obtained behaviourally with the preferential looking technique. Stimulus: stationary gratings, mean luminance 55 cd/m2. Both psychophysical and electrophysiological methods have been applied to study contrast sensitivity of newborns and its development in early life period (see Banks and Dannemiller. 1987. and Mohn and van Hof-van Duin. in press, for recent reviews). The two methods agree in showing that contrast sensitivity is poor in very young infants, and restricted to a band of low spatial frequencies

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(Figure 1, A and B) (Atkinson et al.. 1977: Banks and Salapatek, 1978; Pirchio et al., 1978; Norcia et al. 1988, 1990). During the first six months of life there is a rapid increase in contrast sensitivity, especially a t medium to high spatial frequencies, with a related improvement in visual acuity and a n increase in the optimal spatial frequency (Figure 1. A). Contrast sensitivity at low spatial frequencies (below 1 c/degl remains relatively unchanged with age. Similar findings have been obtained behaviorally in infant monkeys (Boothe et al.. 1980 and 1988). although the time scale of development is different between the two species: one postnatal week for the monkey corresponds to about 4 weeks for the human infant. In spite of the qualitative agreement between the behavioral and the VEP findings on age related changes in the CSF, there are large quantitative differences among the available sets of data. In particular, VEP contrast sensitivities evaluated recently by Norcia et al. (1988,1990)with the swept-contrast technique (Norcia et al., 1985) are much higher than those obtained by others in VEP experiments (Pirchio et al.. 1978; Morrone and Burr, 1986; Atkinson and Braddick, 1989) or using behavioral techniques (Atkinson et al.. 1974; 1977; Banks and Salapatek. 1978). I t is not clear why the swept-contrast technique yields peak contrast sensitivities that consistently exceed those obtained with other methods: psychophysical thresholds coincide with VEP thresholds obtained in the same infant with the Campbell and Maffei ( 1970) extrapolation technique (Atkinson and Braddick. 1989). One possibility is that the function relating VEP amplitude to log contrast in infants is composed of two regression lines of different slopes and that the swept-contrast technique extrapolates to the lower threshold. The two regression lines could represent the activity of two populations of neurons with different contrast sensitivity and contrast gain as described in the monkey (see Kaplan et al., 1990, for review). Other discrepancies can be ascribed to differences in the temporal properties of the stimuli: stationary stimuli were used in two behavioral experiments (Atkinson et al.. 1977; Banks and Salapatek, 1978) and contrast reversal stimuli in the VEP experiments. A temporal modulation of stimulus contrast can facilitate the detection of low spatial frequency stimuli (thus reducing or eliminating the low-frequency fall off). but impair the detectability of high spatial frequencies. If the same temporally modulated stimuli are used in the same infant, the contrast thresholds evaluated behaviorally and with the VEP contrast extrapolation technique coincide (Atkinson and Braddick, 1989). Differences in optimal contrast sensitivity can also be due to differences in mean luminance of the stimuli employed in different experiments: optimal contrast sensitivity can be expected to increase in proportion to the square root of mean luminance in the photopic range and it does so in the adult. The high contrast sensitivities reported by Norcia et al. (1990) have been obtained at luminances exceeding 200 cd/m2, while most of the previous experiments employed luminances of 10 cd/m2 or less. Early behavioral studies on human infants (Atkinson et al., 1977; Banks and Salapatek. 1978) seemed also to indicate that the CSF of one month olds is a low-pass function and that the low-frequency fall off

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typical of adult CSFs shows up later and becomes steeper with age. The adult CSF is thought to result from the sum of several detecting mechanisms with narrower tuning curves and different preferred spatial frequency (see Braddick et al., 1978. for review). The change in the shape of the infant CSF with age has accordingly been ascribed to the progressive maturation of detectors tuned to higher and higher spatial frequencies. This would be accompanied by an increase in contrast sensitivity of the low spatial frequency detectors present already at an early age and possibly by a change from low-pass to band-pass tuning properties. The low-pass shape of the neonatal CSF. however, seems not to be a firmly established fact, a t least for stationary stimuli. [For temporally modulated stimuli, a s typically employed in VEP experiments, the adult CSF has little or no low-frequency decline (Robson, 19661.1 Note that the infant curves of Figure 1A represent VEP amplitudes normalized a t peak contrast sensitivity. No low-frequency fall off has been found in CSF curves obtained by Norcia et al. (1988, 1990) from VEP extrapolated thresholds (see Figure 4. squares) Movshon and Kiorpes (1988) have reanalyzed contrast sensitivity data of human and monkey infants for stationary stimuli and have argued that the reported change in the shape of the CSF with age is probably a n artifact due to group-averaging. By separately analyzing the CSFs of single subjects of the same age they come to the conclusion that the data can be fitted by a function of constant shape, at each age, and that in order to fit the data at different ages it is sufficient to shift the function horizontally and vertically in a log-log plot. If so, it would be unnecessary to invoke the differential development of mechanisms tuned at different spatial frequencies. The development would consist of a scale change brought about primarily by the increase in focal length of the eye and by the change in the spacing of the foveal cones, accompanied by an increase in sensitivity. A similar hypothesis has been advanced by Wilson (1988). who assumes that the development of cortical inhibition also plays a role in sharpening the spatial frequency tuning of single detectors. During infant development, retinal and cortical acuity appear to have a common limiting factor. This is shown by the data reported in Figure 2. The acuities reported in this figure were evaluated from pattern electroretinograms (PERG) and pattern VEPs recorded simultaneously in infants two to six months old. PERG acuities (Figure 2. open symbols) improve with age in parallel with the improvement of acuities extrapolated from VEPs (Figure 2. closed symbols) (Fiorentini et al., 1984). It is generally accepted that limits to visual acuity in infants are mainly imposed by the maturational state of the fovea, and in particular of the foveal cones (Banks and Bennett, 1988: Wilson, 1988; Brown et al.. 1987). although there is no agreement about whether the size and spacing of cones is the only limiting factor. The disagreement derives from slightly different hypotheses on the quantum efficiency of cones in the infant retina. It is difficult at present to resolve this controversial point, because of the few anatomical data available of infant human retinae. Therefore one h a s to consider the possibility that postreceptoral factors also contribute to limit visual acuity, either in the

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retina or in the brain, or both. The data of Figure 2 indicate that postretinal developmental processes possibly involved in the improvement of spatial resolution proceed at the same rate as retinal development during the first six month of life.

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Figure 2. Infant acuities estimated from pattern ERG (open symbols) and VEP (closed symbols) in nine infants. Different symbols represent different subjects. Stimulus: sinusoidal gratings, mean luminance 50 cd/m2, contrast 50%, square-wave contrgst reversal: 6 Hz. Pattern-reversal VEPs are believed to reflect the activity of cortical neurons. In adults, the amplitude of the potentials in response to gratings depend upon the orientation of the grating: it is larger for vertical and horizontal gratings than for oblique gratings (Maffei and Campbell, 1970). This oblique effect is present also in infants starting from 3 months from birth (Sokol et al.. 1987). Since retinal and geniculate neurons of monkeys are not selective for orientation, it is generally assumed that orientational effects in human visual responses indicate cortical processes. Thus, it seems very likely that at three months of age, and possibly before, pattern-reversal VEPs reflect at least in part the activity of cortical neurons and not merely the LGN input to the visual cortex. If so, then the similar trend in the improvement of acuity evaluated from pattern ERG and VEP indicates that acuity of cortical neurons does not lag behind retinal development of acuity. This is consistent with findings on the monkey reported next. In the monkey LGN. the "acuity" of single cells in the foveal representation is low at birth, not exceeding 5 c/deg. During the first

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year of life there is a gradual increase in the spatial resolution of foveal LGN cells (both in the parvo and magnocellular layers) until the mean "acuity" and the "acuity" of the best cells reach adult values of about 30 c/deg (Blakemore and Vital-Durand. 1986). The changes in spatial resolution of LGN cells seem to be related to a progressive decrease in the size of receptive field centers. Interestingly, the spatial resolution of cells in the monkey striate cortex also improves with age, and the improvement in the cortex parallels the improvement in the LGN (Blakemore and Vital-Durand, 1983).Behavioral visual acuity of infant monkeys (Teller et al., 1978; Boothe et al., 1988) increases at a slightly lower rate compared with the acuity of the best cells during the first three months from birth (Jacobs and Blakemore. 1988). Thus in the infant monkey, like in human infants, the development of cortical acuity seems to not lag behind the improvement proceeding at a more peripheral stage in the visual pathway. No data are available so far for the functional development of the retinal ganglion cells of infant monkeys. It has to be noted that in the LGN of the adult monkey, those M cells that show linear spatial summation seem to have similar spatial resolution (on average) as P cells, although cells with the highest acuities (exceeding 25 c/deg) may be more numerous in parvocellular t h a n in magnocellular layers (Blakemore a n d Vital-Durand, 1986). In the parafoveal region of the monkey retina, ganglion cells with sustained response properties seem not to exceed in acuity the resolution of phasic cells (Crook et al., 1988). which project almost exclusively to the magnocellular layers of the LGN. On the other hand, experiments on monkeys with selective degeneration of P cells suggest that the integrity of the P pathway is crucial for reaching a normal behavioral acuity (Merigan and Eskin. 1986; Merigan, 1989: Schiller et al.. 1990). In the newborn monkey the limits to optimal acuity are largely imposed by peripheral factors. The full development of foveal acuity takes a relatively long time in the monkey, as in humans. If the P pathway is mainly responsible for visual acuity in adult monkeys, it is reasonable to assume that in so far as the improvement in acuity reflects changes in the retino-cortical pathway, these changes should eventually involve the P system. As to the contrast sensitivity of P and M cells in infant monkeys. the data available s o far in the literature (Blakemore and Hawken, 1985) indicate that in the LGN the peak contrast sensitivity of the most sensitive P cells approaches adult values even in the neonate. The best M cells are more sensitive than the best P cells, but the difference is less marked than in the adult. Thus, cells in the magnocellular layers must undergo a relatively greater increase in contrast sensitivity during development than cells in the parvocellular layers. These findings might have a bearing on human visual development, as will be discussed at the end of this chapter.

Spatial characteristics: eccentric vision Static and kinetic perimetry show that the visual field of the young infant is small, compared with the adult. In the human newborn the orienting reaction to an object introduced in its peripheral visual

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field is restricted horizontally to within 20 - 30 deg from the fixation point and the vertical visual field is even narrower. The s u e of the visual field remains practically unchanged during the first two months of life (Schwartz et al.. 1987). then increases rapidly to approach adult levels by the end of the first year (see Mohn and Van Hof-Van Duin. in press). Morphologically, the extrafoveal retina of the newborn is relatively more mature than the fovea and its development seems to be complete by the end of the first year of life (Abramov et a1.,1982; Drucker and Hendrickson, 1989). There is unequivocal evidence, however, that peripheral spatial resolution improves after birth (Spinelli et al.. 1983; Sireteanu et al.. 1984; Sireteanu et al.. 19881, rapidly during the first 3 - 4 months and then more slowly. By 3 months of age, but not earlier, acuity is better in the temporal than in the nasal visual field at 20 deg eccentricity (Courage and Adams. 1990) as it is in adults (Rovamo and Virsu, 1979). In the LGN of the adult monkey, spatial resolution of P and M cell declines with eccentricity (Blakemore and Vital-Durand. 1986).At each eccentricity the mean resolution of X-type P and M cells (those that show linear spatial summation) are similar, while Y-type M cells (with non-linear spatial summation) have lower resolution (Blakemore and Vital-Durand. 1986). It seems therefore that the acuity of single neurons depends more on the functional properties of their receptive field (linear vs non-linear summation) than on the P - M classification. On the other hand one has to consider that the retinal ganglion cells that project to the parvocellular LGN layers (defined morphologically as P-beta cells) form the large majority of ganglion cells, while the cells that project to the magnocellular layers (P-alpha cells), are only lW?o of the total population (Perry and Cowey, 1985). Thus the sampling density of P cells largely exceeds that of M cells, and this may assign a predominant role in pattern resolution to the P system. In the newborn monkey, resolution of U ; N cells varies little with eccentricity. The subsequent improvement in resolution with age is prominent in the foveal and parafoveal LGN region, but small at larger eccentricities (Blakemore and Vital-Durand, 1986). This compares well with the larger increase in visual acuity for central vision than for peripheral vision in human infants during the first year (see above).

Temporal characteristics The temporal characteristics of infant vision have not been extensively investigated. Regal (1981) evaluated behaviorally the critical fusion frequency of infants by a forced-choice preferential looking (FPL) method (Teller, 1979). The stimulus was a uniform field square-wave modulated in luminance a t various temporal frequencies, to be discriminated from a non-modulated field of the same mean luminance. The critical fusion frequency (highest discriminable frequency of modulation) was found to increase with age after birth and to reach adult values within three months of age. This is an interesting finding. since in the monkey the sensitivity for fast flickering lights seems to be subserved by the M system (Schiller et al., 1990). More important for vision in a natural environment is the sensitivity to a temporal modulation of contrast in pattern stimuli.

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There has been so far no systematic study of the development of spatio-temporal contrast sensitivity in infants. Some preliminary reports indicate that contrast sensitivity for a fixed spatial frequency is highly dependent upon the temporal frequency modulation of the pattern contrast. The temporal contrast sensitivity function of young infants, however, differs from the adult function, having both lower peak sensitivity and lower optimal frequency. Moreover, the low-frequency fall off in sensitivity characteristic of adult functions does not appear until 3 - 4 months of age (Hartmann and Banks, 1984; Swanson and Birch, 1989). Again, it is of interest to investigate whether the temporal characteristics of the neonatal visual system are constrained mainly at a retinal or at a higher level. Some information can be obtained from simultaneous recording of the pattern ERG and VEP (Fiorentini and Trimarchi, 1989). Temporal resolution evaluated from the PERG for gratings of low spatial frequency (0.5 c/deg) sinusoidally reversed in contrast, improves with age between 2 and 5 months of age, as it does for the pattern VEP. The function relating PERG amplitude to temporal frequency of contrast reversal is practically low-pass at 6 weeks of age and tends to become more band pass between 2 and 5 months from birth. The same is true for the temporal tuning function of the pattern VEP (Moskovitz and Sokol, 1980). [It has to be noted that these functions do not describe contrast sensitivity, but the dependence of response amplitude from temporal frequency for a constant stimulus contrast.] At each age there is a tendency for the PERG to peak at a higher frequency and to have a hlgher temporal resolution than the pattern VEP (Fiorentini and Trimarchi. 1989) as occurs for the adult (Plant, Hess and Thomas, 1986). Thus the development of temporal frequency characteristics for contrast reversal seems to be constrained by postretinal limiting factors, in addition to the limits imposed by retinal immaturity. If we had better knowledge of the complete spatio-temporal CSF in infants and of its changes with age, it would be possible to compare the development of sensitivity for temporal contrast modulation with the development of visual acuity. This might be relevant to the question of possible differential development of P and M pathways. In view of the findings obtained from behaving monkeys with selective destruction of P-beta ganglion cells (Merigan and Eskin. 1986: Merigan. 1989) and also on t h e basis of electrophysiological properties of P and M cells, there seems to be general consent that contrast sensitivity for temporally modulated patterns of low spatial frequencies is subserved by M cells, while spatial resolution tasks are mediated by P cells (Kaplan et al., 1990: Lennie et al., 1989). Unfortunately the developmental data about temporal frequency characteristics available so far are still incomplete. The data obtained from VEP experiments which typically employ gratings reversed in contrast at 5-8 Hz. indicate that contrast sensitivity for low spatial frequencies matures quite early compared with spatial resolution (Pirchio et al.. 1978. Norcia et al., 1990). It would be of interest to know how these flndings compare with the development of contrast sensitivity at low spatial frequencies for stationary patterns, but the data on psychophysical CSF available so far cover only the earliest postnatal months (Atkinson et al., 1977;

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Banks and Salapatek, 1978) or a much later range of preschool ages (Beazley et al.. 1980; Atkinson et al.. 1981). At what age the CSF for stationary stimuli is fully developed is still unknown. Several studies have been devoted to the development of VEP responses to transient contrast reversal. In the adult, these transient VEPs have a rather complex waveform, with a main positive deflection that peaks with a delay of about 100-110 ms with respect to stimulus reversal. In the newborn infant, the waveform is much simpler and the positive wave peaks with a much longer delay (around 250 ms or more). The peak latency shortens rapidly after birth and for checkerboard patterns with large checks it levels off at adult values towards the end of the first year. For small checks the peak latency decreases at a lower rate and takes longer to reach adult values (Moskowitz and Sokol, 1980). 300

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Figure 3. Peak latency of the pattern VEP (solid symbols) and ERG (open and stippled symbols) as a function of age. Different symbols represent different subjects. Stimulus: sinusoidal grating, 0.5 c/deg, contrast 50%. square-wave reversed in contrast a t 1 Hz, mean luminance 50 cd/m2.

The long latencies observed in the transient VEPs of young infants are likely to reflect the sluggish response properties of neonatal visual neurons (Blakemore and Vital-Durand, 1986) in addition to the slower conduction velocities of visual nerve fibers. Comparison

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with the PERG in response to transient contrast reversal of low spatial frequency gratings is indicative of both these facts. The peak latencies of the neonatal ERG (Fulton and Hansen, 1982. 1989) and PERG (Fiorentini and Trimarchi. 1989) are also much longer than the adult's, suggesting that the neonatal photoreceptors and retinal neurons are also sluggish. However, PERG latency decreases during early infancy (Figure 3, open and gray symbols) and approaches adult values earlier than the VEP latency (Figure 3,closed symbols) (Fiorentini and Trimarchi, 1989). This suggests that retinal circuitry develops more rapidly than cortical circuitry. Latencies of the responses of single neurons to visual stimulation have been measured in the LGN of macaque monkeys of various ages from birth to adulthood (Blakemore and Vital-Durand, 1986). The latency of the responses is much longer in newborn monkeys compared with adults. It extends u p to 150 ms and even the shortest latencies are longer than the longest latencies of adult LGN

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Figure 4. Contrast sensitivity a t three luminance levels estimated from VEP recorded from adults (A) and infants 10 weeks old (B).Data obtained at 0.06 and 6 cd/m2 from one adult and one infant subject have been replotted from Fiorentini et al. (1980) Stimulus: sinusoidal gratings square-wave reversed in contrast a t 8 Hz. The data a t the highest luminance are means of five adults and ten 10-week-old infants, Stimulus: sinusoidal gratings reversed in contrast at 6 Hz.

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cells. Then latencies decrease rapidly and consistently and approach adult levels around 70 days of age. There is a tendency for cells in the magnocellular layers to have shorter latencies than parvocellular cells a t all ages. This fact probably reflects the higher conduction velocities of P-alpha cell axons.

Scotopic vision The properties of scotopic vision of young infants indicate that the rods, although not yet morphologically mature (Drucker and Hendrickson. 1989). are functional in the human neonate. The scotopic spectral sensitivity function of 1 and 3 month old infants practically coincides with the adult function and the absolute sensitivity is only 1.7-2 log units below adult sensitivity at 4 weeks and 0.7-1 log unit at 3 months (Powers et al., 1981; Hansen and Fulton, 1987). So far, there has been only one study of infant contrast sensitivity a t low luminance levels (Fiorentini a t al., 1980). These VEP data (Figure 4 B. filled circles) indicate that a t 10 weeks of age, contrast sensitivity for sinusoidal gratings of low luminance (0.06 cd/m2) reversed in contrast at 8 Hz is lower than the adult sensitivity (Figure 4 A. filled circles) and the same is true for acuity. Psychophysical data also show that a t 2 months visual acuity is lower than adult acuity at all luminance levels (Brown et al.. 1987). The difference in contrast sensitivity between infants and adults, however, is rather small (a factor of 2 - 3) and adult values are reached within 4 months from birth (Fiorentini et al., 1980). Figure 4 also compares CSFs obtained in adults and 10 week old infants a t a low photopic (open circles) and a high photopic level (closed squares) with the low-luminance CSF. Interestingly, the optimal contrast sensitivity of adults increases in proportion of the square-root of mean luminance. For infants, the contrast sensitivities of the two extreme sets of data (obtained in different laboratories) are also in agreement with the square-root law, while the data for the intermediate luminance deviate consistently from this law. This point is of interest and will be reconsidered in the Discussion. Summation properties of the infant scotopic visual system are also different from the adult, both in space and time. Area summation is about 12 times the adult's a t 4 weeks and 4 times the adult's a t 11 weeks (Hamer and Schmeck, 1984). Temporal summation also extends over much longer stimulus durations in 10 week old infants than in adults (Hansen and Fulton, 1990) and the temporal summation function is very shallow in young infants, suggesting that the inhibitory components of the temporal response function are delayed or less pronounce than in the adult (Fulton, 1988). In conclusion, receptoral and preneural factors seem insufficient to explain the immaturity of scotopic vision at birth and its subsequent development. Most of the developmental processes are likely to be due to changes occurring in visual structures central to the photoreceptors.

Spatial frequency selectivity In the adult monkey, a large proportion of cells in the LGN and in the striate visual cortex have band pass spatial frequency

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characteristics (Kaplan and Shapley, 1982: Derrington and Lennie, 1984; Blakemore and Vital-Durand, 1986; Poggio et al., 1977: DeValois et al., 1982: Foster et al. 1985). In human subjects, psychophysical and electrophysiological evidence indicates that visual detectors are selective to limited bands of spatial frequencies (see Braddick et al.. 1978. for review). There are few data that describe the development of spatial frequency tuning of single cells in the monkey visual system. Blakemore and Vital-Durand (1986) report various examples of response curves

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Figure 5 . Spatial frequency channels: effects on the amplitude of the VEP in response to a sinusoidal grating of constant spatial frequency (arrow) and moderate contrast ( 15-20%). square-wave reversed in contrast at 7 Hz. in the presence of a masking grating of high contrast, reversed in contrast at 6 or 9 Hz. Mean luminance: 6 cd/m2. A adult data for 4 different spatial frequencies of the test stimulus. B: data from an infant 1 1/2 months old. C: data from an infant 3 1/2 months old. Different symbols indicate different experimental sessions.

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of LGN cells as a function of stimulus spatial frequency, recorded from infant monkeys at different times from birth. In very young animals the responses of single cells peak at relatively low spatial frequencies and the high frequency cut off does not exceed 5 c/deg. However, the response functions show a clear low-frequency attenuation. Thus at least some LGN neurons have band pass spatial frequency characteristics even in the newborn monkey. The tuning then sharpens with age and the optimal spatial frequency a s well as the cut-off of the best resolving cells move toward higher spatial frequencies. These findings are relative to P cells. No data are available for the tuning characteristics of M cells in the infant monkey. Very little is known of the tuning characteristics of cortical neurons of infant monkeys. There seems to be some indication that in very young animals the spatial frequency tuning characteristics of cortical neurons have little low frequency attenuation (Blakemore and Vital-Durand, 1983). The same is true in young kittens (Derrington and Fuchs, 1981). There have been two attempts to find evidence for spatial frequency channels in human babies, both using a masking procedure. One study (Fiorentini et al., 1983) reported spatial frequency selective effects of masking on the amplitude of VEPs in response to sinusoidal gratings of fxed spatial frequency, reversed in contrast a t 7 Hz. The masking grating had a variable spatial frequency, either lower or higher than the test grating, and was reversed in contrast a t a slightly different temporal rate. The amplitude of the VEP in response to the test stimulus was reduced in the presence of the masking stimulus by a n amount that depended upon the difference in spatial frequency between the two stimuli (Figure 5). The second study (Banks. Stephen and Hartmann. 1985) applied the psychophysical preferential looking technique to investigate the effects of a narrow-band noise masker on the detectability of sinusoidal gratings of three different spatial frequencies. The two studies agree in showing that spatial frequency selectivity is present in infants 3 months old. The bandwidth of tuning at 1 c/deg at this age (Figure 5, C)is comparable to that of adult tuning for higher spatial frequencies (Figure 5, A). This finding can be understood in terms of the different spatial scales in the infant and adult foveae (Wilson, 1988). For younger infants, there is disagreement between the electrophysiological and the psychophysical studies. While in the former the data from one infant 6 weeks old show band pass tuning a t 0.3 c/deg (Figure 5. B). in the latter the average results of five 6 week old infants indicate low pass tuning. Whether this discrepancy is due to the small sample tested, to group averaging or to methodological differences remains to be investigated. One possible reason could be found in the different temporal properties of the test stimuli used in the two experiments. Possibly, band pass spatial frequency tuning may become manifest at an earlier age with temporally modulated than with stationary stimuli because of different developmental rates of mechanisms with different temporal response properties. It has also to be noted that, because of the contrast gain of the visual system (see for instance Figure 8), the effects of a masking stimulus on the contrast threshold (FPL experiment), may be expected to be considerably smaller than the effects on the response to a stimulus of suprathreshold contrast (VEP experiment).

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Vernier acuity Vernier acuity (the ability to detect the misalignment of two abutting lines or gratings) is a type of hyperacuity. In foveal vision, adults vernier thresholds can be an order of magnitude better than thresholds for grating resolution. In peripheral vision on the contrary, vernier acuity drops much more steeply than grating acuity with increasing eccentricity (Westheimer, 1982: Levi et al., 1985). Having in mind the very small foveal thresholds for hyperacuity tasks in adults, one may be surprised to learn that in young infants vernier acuity evaluated behaviorally is lower than grating acuity (Shimojo and Held, 1987). This situation reverses rapidly, however, because vernier acuity develops at a higher rate than grating acuity (Figure 6. A). Already a t 3 to 4 months of age vernier acuity exceeds grating acuity (see Gwiazda et al.. 1989a for review). A difference in the rate of increase of grating acuity and vernier acuity can be expected merely on the basis of preneural factors, in particular of the quantum efficiency of the photoreceptors (Geisler, 1989: Banks and Bennet, 1988). That this is not the whole story, however, is suggested by two interesting facts about the development of vernier acuity. First, there is a sex difference in the rate of improvement of vernier acuity. Between 3 and 5 months females are better in vernier acuity than males (Held et al.. 1984). No sex difference is observed for the development of grating acuity. Second, vernier acuity continues to improve in children up to 7 years of age (Figure 6B, squares). while grating acuity levels off much earlier (Figure 6B, circles). Apparently, the development of vernier acuity requires the maturation of structures or the development of processes beyond those responsible for the age related increase in grating acuity. Perhaps all these factors mature simultaneously during an early life period, so that grating acuity and vernier acuity appear to have the same limiting factors. A differential time course in the development of vernier acuity and grating acuity has been found also in infant monkeys (Kiorpes and Movshon, 1989).These findings parallel those in human infants, apart from the different time scale.

Binocular function and stereoacuity Like most spatial acuities that develop gradually after birth, stereopsis seems to emerge abruptly between 3 and 4 months of age. After this sudden onset, stereoacuity increases very rapidly during the next few weeks, to reach thresholds as low as 60 arcsec around six months of age (see van Sluyters et al., 1989, for review). Several years seem then to be required for stereoacuity to match adult values (Gwiazda et al.. 1989a). Simultaneously with the onset of stereopsis there is evidence for the onset of another binocular function: infants start to prefer binocularly fusible stimuli to stimuli that in the adult produce binocular rivalry (such as vertical stripes in one eye and horizontal stripes in the other) (Shimojo et al.. 1986: Gwiazda et al., 198913). Other forms

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Figure 6. Development of grating acuity, stereoacuity and vernier acuity in infants (A1 (top panel) and children (B) (bottom panel). Vernier

acuity and stereoacuity for some older infants (A). older children and adults (B)were limited by the maximum resolution of the display. Copyright 1989. Canadian Psychology Association. Reprinted by permission.

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of binocular function have been investigated in infants, for instance the preference for random-dot stimuli correlated in the two eyes with respect to non-correlated stimuli. There is some controversy on whether this preference appears concomitantly with the onset of stereopsis (Smith et al., 1988) or appears earlier (Einzeman et al., 1989).

As for vernier acuity, there is a sex difference for the development of stereoacuity and of fusion preference (Bauer et al. 1986: Gwiazda et al., 1989a). Females show evidence for stereopsis and for fusion preference around 9 - 10 weeks, while males do not before 12 - 13 weeks. The sudden appearance of stereopsis and fusion around 3 months of age has been suggested to reflect the process of segregation of monocular inputs to layer IV in the striate cortex (Held. 1985). There is some evidence that this should occur between 4 and 6 months in human infants (Hickey and Peduzzi. 1987). It seems rather unlikely however that the segregation process is confined to a very brief period of time. Possibly segregation of monocular inputs is a necessary prerequisite for binocular stereopsis, but other factors are involved.

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age 7 w e e k s

Figure 7 . VEP responses to orientation reversal of a grating pattern in a 7 weeks old infant (b). The lower trace represent the timing of

stimulus reversals. The upper trace (a) represents for comparison VEPs recorded in response to appearance of a pattern. Reprinted by permission from N a t u r e , Vol. 320, p.618. Copyright (C) 1986 Macmillan Magazines Ltd .

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Discrimination of orientation In the newborn monkey, cells in the visual cortex show a considerable degree of orientation specificity a n d a system of orientation columns is already established a t birth (Wiesel and Hubel. 1974). Since in higher mammals specificity for orientation is a property of cortical neurons that is not shared by neurons at lower levels of the visual system, it is of interest to know whether the human visual system also shows some kind of sensitivity for orientation of lines or contours. Two lines of research have been followed to investigate orientation discrimination in infants. Behavioral experiments based on the habituation paradigm (Maurer and Martello. 1980) provide evidence that human neonates can discriminate square wave gratings oriented a t 90 deg from each other (Slater et al., 1988). The selectivity for orientation however is probably rather poor at birth. In the adult it is possible to evaluate the width of orientation channels using a masking procedure (Campbell and Kulikowski. 1966). Experiments applying the masking technique to babies of various ages suggest that tuning for orientation is very poor at one month of age, but that it improves between 2 and 4 months and remains constant thereafter (Held et al.. 1989). On the whole, these behavioral experiments indicate that orientation selectivity is a t least to some degree innate and that it probably reaches adult values much earlier than other visual functions. Somewhat different findings have been obtained following another line, namely by recording VEPs in response to patterns that periodically change in orientation (Braddick et al.. 1986). Responses correlated with 90 deg shifts in orientation of the stimulus grating, occurring 8 times per second (Figure 71, could be recorded in infants 6 weeks old, but not in younger infants. It appears, however, that the age of onset of orientation-specific VEPs depends on the temporal rate of orientation-reversals. For reversals occurring 3 times per second, VEP responses could be obtained in infants 3 weeks old, earlier than for a 8 Hz rate of reversal (Braddick et al., 1989). This was confirmed using the habituation paradigm: at one months of age infants are sensitive to 90 deg shifts of orientation if these occur at a rate of 3 Hz. but not a t a rate of 8 Hz. These findings seem to recompose the apparent controversy between behavioral and electrophysiological studies of orientation discrimination in very young infants. Probably the VEP responses to a change in stimulus orientation reveal the relative immaturity of temporal characteristics of orientation selective neural mechanism. Both sets of results are consistent with the presence of some form of orientation discrimination very early in life. And both provide evidence that orientation selectivity improves rapidly after birth, approaching adult values by 3 - 4 months of age (Atkinson et al.. 1988; Held et al., 1989). It is possible, however, that the psychophysical experiment, based on masking effects, reveals the development of inhibitory interactions that are not necessarily involved in the VEP experiment.

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Motion Perception Motion perception has been studied in infants both psychophysically and electrophysiologically. Psychophysical studies using the preferential looking procedure indicate that infants of 3 months of age and older show a preference for a moving with respect to a stationary pattern, provided the pattern velocity exceeds a threshold (see Dannemiller and Freedland. 1989). In 3 - 4 months old infants the minimum velocity threshold for drifting gratings of low spatial frequency is of the order of 3 - 5 deg/s (Aslin. 1988: Dannemiller and Freedland. 1989). Infants of 2 months or younger either do not show any preference for a moving stimulus (Dannemiller and Freedland, 1989) or have very poor sensitivity to motion. at least at low velocities (Kaufmann et al., 1985). VEP studies agree with the behavioral findings indicating a relatively late development of motion sensitivity. A VEP response to motion can be obtained by reversing at a fixed temporal frequency the direction of motion of a random dot pattern (which also jumps incoherently a t and between reversals a t a high temporal frequency). Responses time-locked to the reversals of motion direction, and not to the intervening jumps, are considered to reflect the activity of mechanisms sensitive to the direction of motion, and not simply to pattern change (Wattam-Bell, 1987).In adults, motion specific VEPs are recordable in a large range of stimulus velocities (5 to 30 deg/s). and peak around 15 deg/s (Wattam-Bell. in press). In infants younger than 10 weeks, no motion specific responses are recordable, even at low velocities (5 deg/s), although responses to the pattern jumps are clearly present. Motion specific VEPs emerge around 10 weeks of age at low velocities, but still later for stimull of higher velocity. The highest velocity at which a motion-specific VEP is obtained increases with age (Wattam-Bell, in press). Oculomotor responses are also rather immature in very young infants. For instance, smooth pursuit can be observed around 10 weeks of age for linear motion of a target at low velocities (Shea and A s h , 1988) but not at higher velocities, where it is replaced by a series of saccadic eye movements (Aslin. 1987). Optokinetic responses are immature at birth: monocular optokinetic nystagmus (OKN) can be elicited by stimuli moving in the temporal-nasal direction, but not in the opposite direction (Atkinson. 1979). I t is not until after 3 months of age that the monocular OKN can be driven in either direction. The immaturity of smooth pursuit can be explained at least in part by the lack or immaturity of motion perception. The OKN asymmetry has been ascribed to the lack of appropriate cortical inputs to the motor centers responsible for the optokinetic response (Atkinson, 1984; van Hof-van Duin.1978). In conclusion, both sensory and oculomotor responses to moving stimuli seem to be immature a t birth and to emerge somewhat later in comparison with other visual responses. If a longer age span is considered, however, it appears that motion specific responses may complete their maturation years in advance to some pattern specific responses (De Vries et al., 1989).

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Inhibitory interactions Inhibition plays a crucial role in shaping the response of single visual neurons and in controlling the interplay of stimulus evoked activity in different neurons. Signs of inhibitory phenomena in the intact visual system of adult human subjects are found for instance in subthreshold interactions, in masking phenomena and in the low-frequency cut off of the CSF. In cats, surround inhibition in retinal and LGN receptive fields is present, but weak, a t birth and it develops gradually during the early postnatal period (Hamasaki and Flynn. 1977;Rusoff and Dubin. 1977:Berardi and Morrone. 1984). Inhibition must be present at least to some degree in the LGN neurons of the neonatal monkey, because their spatial frequency tuning characteristics are band pass in shape (Blakemore and Vital-Durand, 1986).Apparently, this type of inhibition is less mature in the neonatal visual cortex (Blakemore and Vital-Durand. 1983). 1 16

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Figure 8. Development of cross-orientation inhibition in one infant at three different ages. VEPs in response to contrast-reversal of a

sinusoidal grating of low spatial frequency are plotted against the stimulus contrast (circles). The other symbols indicate VEPs in response to the same stimulus in the presence of a masking grating reversed in contrast at a different temporal frequency and either parallel (squares) or orthogonal (triangles) to the test grating. Note that at 4 months the parallel mask, but not the orthogonal mask, attenuates significantly the VEP, indicating orientation selectivity at that age. At 10 months, both the parallel and the orthogonal masks affect the VEP amplitudes, though in different ways, as occurs in the adult. Reprinted by permission from Nature, Vol. 321, p.235. Copyright (C) 1986 Macmillan Magazines Ltd. In human infants we have seen that some type of inhibitory phenomena are present at an early age. For instance, it is possible to suppress the response to a grating of a certain spatial frequency by

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101

a mask of a different spatial frequency, but the masking effect is less strong than in the adult (Fiorentini et al., 1983; Banks et al., 1985). The CSF of young infants was reported to be low pass in shape, but probably this is an artifact due to not having used sumciently low spatial frequencies. Effects revealed by VEPs in response to complex visual stimuli, attributed in the adult to lateral inhibitory interactions, seem to be present in 8 week old infants (Sokol, Zemon and Moskowitz, personal communication). There is evidence, however that more subtle inhibitory effects, such as those that occur between orthogonal gratings at suprathreshold contrasts, do not emerge until six to eight months of age (Figure 8) (Morrone and Burr, 1986). This phenomenon, known a s "cross-orientation inhibition." is present in single cells of the cat visual cortex (Morrone et al.. 1982) and is believed to reflect GABA-mediated interactions among cells tuned to different orientations (Morrone. Burr and Speed, 1987). Also VEPs evoked by windmill-dartboard stimuli, that in the adult have been attributed to short-range lateral interactions (Zemon and Ratliff. 1982) do not appear earlier than 5 months from birth, and are still very immature at this age (Moskowitz and Sokol, 1989). The development of interactions between orthogonal stimuli and other types of complex stimulus interactions probably require the refinement and progressive selectivity of horizontal connections in the visual cortex, like those observed in visual cortical areas of the monkey (see Gilbert, 1985 for a review). These have been found to develop after birth (Burkhalter and Bernardo. 1989) and may rely upon the development of dendritic trees in the upper cortical layers (Becker at al. 1984) a s well a s in the progressive selectivity of intracortical synaptic connections, likely to start around the 8th month of age (Garey and de Courten. 1983).

Color vision The development of color vision in infants has been recently reviewed by Teller and Bornstein (1987). They conclude their overview of all the relevant literature with a few important established facts. First, photopic and scotopic spectral sensitivities are mature within the first or second postnatal month. Second, infants in the second month of life have trichromatic color vision, since they can do both Rayleigh discriminations (and therefore are neither protanopes nor deuteranopes) and tritan discriminations (and therefore must have a third type of cones, sensitive to short wavelengths). The three cone types with highest sensitivity in the long (L),medium (M) and short (S) range of wavelengths, respectively, are likely to have spectral absorption properties not dissimilar to adult photopigments. Third, infants 4 months old categorize wavelengths of the visible spectrum much in the same way as adults. Infant categorization is based on a habituation-dishabituation paradigm and grouping occurs for four ranges of wavelengths corresponding to the spectral regions that adults categorize a s blue, green, yellow and red, by hue naming (Bornstein et d., 1976: Boynton and Gordon, 1965). However, neonates and very young infants (3 weeks old) seem to have an immature S cone system Warner et al., 1985; Adams et al..

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1986). Moreover, 3-week-old infants fail to discriminate monochromatic lights (at mesopic luminances) that are discriminated by 7-week-olds (Clavadetscher et al.. 1988). Thus the ability to discriminate colors, a t least under mesopic conditions, emerges between 3 and 7 weeks from birth. Color vision seems therefore to develop early in infants and to have the main characteristics of trichromatic vision. This general statement is supported by further experimentation, that has also

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test wavelength (nm) Figure 9. Detection thresholds for various monochromatic lights on a monochromatic (580 nm) adapting background, obtained with the preferential looking procedure in 3 months old infants (circles) and with the yes-no procedure in adult subjects (triangles). The 8 deg circular stimulus was either sharply focussed (closed symbols) or blurred (open symbols). The arrows indicates the adapting wavelength.

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uncovered other important aspects of color vision. Brown and Teller (1989) report a n interesting experiment in which the spectral sensitivity of 3 month old infants was evaluated a t five different wavelengths in the range 540 - 650 nm. In the middle of this range the spectral sensitivity curve presents a notch, like in adults, that reflects the non-additivity of responses of L and M cones (Figure 9). These findings are consistent with a color-opponent model. Therefore they provide evidence that at 3 months from birth, color-opponent mechanisms can be functional (with the caveat that infant color opponency has not been proven identical to adult opponencyl. Heterochromatic flicker photometry, a means to evaluate photopic spectral sensitivity, is usually performed with uniform field illumination. Anstis and Cavanagh (1983) have devised a technique for matching the luminances of gratings of different colors. The gratings are presented temporally in such a way to produce apparent motion in one or the other direction, according to their relative luminances. In adults this method yields spectral sensitivity curves equivalent to those evaluated with flicker photometry. Its usefulness for infant testing comes from the fact that patterns that are not isoluminant produce optokinetic nystagmus in either direction, while a t isoluminance the pattern appears practically stationary, and no OKN is elicited. Thus isoluminance can be determined by observing the presence and direction of optokinetic eye movements of infants. Application of this method (Maurer et al., 1989) and a variant of it (Teller and Lindsey, 1989) have confirmed that relative spectral sensitivities of 1 to 3 months old infants are remarkably similar to those of adults. It is important to recall, however, that the conditions of the motion-nulling OKN technique are likely to reveal the properties of a photopic mechanism of the peripheral retina. Previous disagreement about a difference between infant and adult spectral sensitivity curves in the short wavelength region of the spectrum may derive from methodological differences. Another possible reason is the lower density of ocular media of infants compared with adults. Hansen and Fulton (1989) measured absolute sensitivity a t the short wavelength end of the spectrum (401 nm) as well as a t 561 nm, in 10 week old infants. Comparison of the sensitivities at the two wavelengths in infants and adults showed that infants are relatively more sensitive than adults at 401 nm. Since human rhodopsin absorbs these two wavelengths equally well, the difference between infants and adults has to be ascribed to a higher optical density of the adults' eye at 401 nm. Most of this difference is probably due to the lens and is likely to decrease progressively with age. In conclusion, there is convergent evidence that the photopic spectral sensitivity of young infants is very similar to that of the adult and that in the second month from birth three types of cones are active and some color discriminations are possible. This does not a t all mean that color vision is completely developed at this age. For instance, infant color discriminations require large color contrast and also stimuli of large size (Packer et al., 1984; Adams et al.. in press). This suggests that the spatial characteristics of the infant color system are different from those of the adult.

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Spatial and temporal characteristics of color contrast sensitivity Visual potentials evoked by chromatic stimuli have offered a means to investigate the development of color contrast sensitivity in infants, both in the spatial and temporal frequency domain (Morrone et al., 1989). The stimulus was a periodic pattern obtained by superimposing two sinusoidal gratings of the same spatial frequency at crossed orientations. It appeared as a plaid pattern with very blurred contours. Two such patterns were generated by the red and the green guns of a T V monitor, and either presented separately or superimposed with a 180 deg spatial phase shift, to form a red-green plaid. The relative luminances of the red and green components could be varied at will, from 100% red to 100% green, while keeping constant the total mean luminance and the equal contrasts of the two components. If the proportion of red to green is varied continuously, a value of this ratio has to be such that the red and green components are matched in brightness. This is the so-called isoluminant point.

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Figure 10. VEP amplitude as a function of the ratio of red-to-total mean luminance in the stimulus pattern. A: adult subject, 1 c/deg stimulus, mean luminance: 16 cd/m2, contrast: 30%. square-wave reversal: 7.5 Hz. B and C: infant PAB, at two ages. Stimulus spatial frequency: 0.1 c/deg. mean luminance: 16 cd/m2, contrast: 90%, square-wave reversal rate: 2 Hz (B),3 Hz (C). In adults, plaid patterns reversed in contrast (at a temporal frequency of say 5 - 6 Hz) evoke a second harmonic VEP response for any value of the ratio of the red luminance to the total luminance. At relatively low contrasts, the VEP amplitude has a minimum for the ratio corresponding to the isoluminant point, a s determined by flicker photometry (Figure 10. A). Similarly to what is done with the

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pattern-reversal VEPs in response to luminance contrast, it is also possible to evaluate a contrast threshold by extrapolation of VEP amplitude against chromatic (isoluminant) contrast. This threshold coincides with the psychophysical contrast threshold. Not surprisingly, therefore, application of this method to adults yields contrast sensitivity curves for chromatic contrast that are very similar in shape to those obtained psychophysically (Mullen, 1985). This method has been applied recently to investigate the development of chromatic contrast sensitivity in infants (Morrone et al.. 1989). Chromatic VEP responses to patterns of very low spatial frequency (0.1 c/deg) reversed in contrast a t a low temporal frequency do not emerge prior to 5 to 7 weeks of age (Figure 10, B and C). Responses at higher spatial and temporal frequencies have a later onset. Chromatic contrast sensitivity increases progressively with age between 2 and 6 months and approaches adult values before contrast sensitivity to luminance modulated patterns of the same spatial and temporal low frequencies (Figure 11. top). The same is true for chromatic acuity, i.e. the highest spatial frequency a t which a chromatic (isoluminant) VEP can be obtained: with the emergence of chromatic responses it increases more rapidly than VEP acuity for isochromatic, luminance modulated gratings (Figure 11, bottom). Sensitivity for chromatic contrast with isoluminant patterns is relatively low because of the broad and largely overlapping action spectra of the photopigments. This fact together with the immaturity of photoreceptors in the infant retina has been considered to be the main factor responsible for the difference between contrast sensitivity for luminance- and color-contrast in young infants (Banks and Bennett, 1988). However, other factors must play a role in the development of infant chromatic contrast sensitivity, since the rate of increase in sensitivity with age is different for chromatic and luminance contrast. It is likely that mechanisms responsible for encoding and processing color information a t post receptoral levels, e.g. color opponent receptive fields, are immature a t birth and develop later, at least in part independently from developmental processes involved in the increase of luminance contrast sensitivity with age. A recent report seems to disagree with this conclusion, however. Using the VEP swept contrast technique (Norcia et al., 1985) for evaluating contrast sensitivity, Allen et al. (1990) report that the contrast sensitivity for isoluminant stimuli has the same ratio as the sensitivity for luminance contrast in young infants and adults, suggesting that the reduced infant sensitivity results entirely from preneural factors. Further investigation seems to be required to resolve this controversy.

Discussion Not all possible aspects of human visual development have been covered in this chapter. For instance, visual attention, recognition of complex shapes or other cognitive aspects of vision have not been considered. Still, the picture that emerges from the previous sections is rather complex. The reader will be easily convinced that, as anticipated in the introduction, there is usually little ground for ascribing this or that aspect of human visual development to the maturation of one or

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Figure 11. Contrast sensitivity for a low spatial frequency (A)and acuity (B),evaluated from VEPs in response to red-green isoluminant gratings (open symbols) or to isochromatic (red-black or green-black) gratings (closed symbols) reversed in contrast at a low temporal frequency, plotted against age, for a group of infants 5 to 30 weeks old. Different symbols indicate different infants. Each point was obtained by extrapolation to zero amplitude of VEP amplitudes plotted against stimulus contrast (top) or spatial frequency (bottom). Points below the unit contrast sensitivity in the top graph indicate infants and ages at which no significant VEP could be obtained with isoluminant stimuli, although a t the same age VEPs in response to luminance-contrast reversals were clearly present.

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another neuronal population. I t is clear, however, that different visual capabilities may emerge at different times after birth and that different visual functions may show different developmental trends. And there is convergent evidence from morphological and behavioral findings that postnatal visual development in human infants proceeds both serially, at subsequent stages of the visual pathways, and in parallel, along dffferent neural streams. There have been recent proposals to differentiate an early phase of visual development, dominated by retino-tectal structures, from a later phase, when cortical functions become predominant and the visual activity mediated by the cortex starts to control the subcortical visuomotor functions (see Atkinson. 1984). This two-stage developmental process accounts for some facts, such as the separate emergence of the two opposite directions of OKN. but it comes u p against the fact that newborns can discriminate patterns of different orientations. This behavioral performance has to rely upon neural mechanisms that respond selectively to different orientations. Orientational selectivity is a property of cortical neurons that is not shared, at least in non-human primates, by tectal neurons. Thus it has to be recognized that the visual cortex is active to some degree even in the newborn, though possibly very immature. Before discussing the possible functional effects of maturation at a cortical level, let u s consider those aspects of vision that may be determined primarily by the development of structures peripheral to the visual cortex. This is the case, for instance, for visual acuity and spatial contrast sensitivity. There seems to be general consent that contrast sensitivity for temporally modulated patterns of low spatial frequency is mediated by the M retino-cortical pathway, while color contrast sensitivity is subserved by cells in the P pathway (Merigan. 1989: Kaplan et al., 1990; Schiller et al.. 1990: Mollon, 1990). Scotopic pattern detection may imply primarily the activity of the M stream (Kaplan et al.. 1990). Now, the contrast sensitivity for temporally modulated patterns of spatial frequency less than 1 c/deg develops early (Atkinson et al.. 1974: Harris et al.. 1976: Pirchio et al., 1978: Norcia et al., 1988, 1990) and at low luminances contrast sensitivity matches adult values earlier than at higher luminances (Fiorentini et al., 1980).This may be ascribed to a n early functional maturation of M cells. On the other hand, if we consider how the contrast sensitivities for luminance and color contrast increase with age (Figure 10) it is tempting to jump to the conclusion that the development of the P system is somewhat delayed, but more accelerated with respect to the M system. While the findings of Figure 10 are not inconsistent with this interpretation, other factors have to be taken into account. First, as mentioned in the previous section, the delayed onset of responses to color contrast compared with luminance contrast (Morrone et al., 1990) may be a consequence of the spectral properties of the photoreceptors: the largely overlapping action spectra of the L and M cones impose a limit to the maximum attainable color contrast. Thus, what might appear to be a delayed emergence of the neural system mediating color contrast sensitivity can largely be accounted for by preneural factors (Banks and Bennett, 1988). The different slopes of the two developmental curves of Figure 10. on the contrary, cannot be

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accounted for by preneural factors, because these should affect by the same amount the sensitivities for luminance and color contrast. Secondly, a word of caution h a s to be said about the interpretation of contrast reversal VEPs in terms of separate contributions from the P and M systems. The steady-state VEP responses to contrast reversal, either luminance contrast or color contrast, contain only the even harmonics of contrast modulation and therefore represent non-linear components of the response. Second harmonic non-linearities have been observed in the responses of monkey M ganglion cells to flickering red-green uniform lights matched in luminance and have been ascribed to non-linear interactions between the L- and M-cone inputs to the non-color opponent M cells (Lee et al.. 1989). Before more is known about the neural origin of contrast-reversal VEPs, it would be premature to ascribe the isoluminant contrast-reversal VEPs exclusively to the P system. Some promising results for the differentiation of pure color-contrast VEPs from responses to luminance-contrast are being obtained from patterns modulated in contrast in the on-off mode a t low temporal frequencies (Fiorentini et al., 1990). The preliminary findings of these experiments are consistent with those obtained with pattern-reversal isoluminant V E P s indicating a differential development of color- a n d luminance-contrast responses. As to contrast sensitivity a t medium and high spatial frequencies, there is no general agreement whether in the adult this is subserved mainly by the M or the P system. I t is in this range that the infant data obtained under different experimental conditions differ mostly (see for example Figs. 1 and 4). In particular, VEP contrast sensitivities obtained with the swept-contrast technique are much higher than those obtained in a number of different laboratories with the extrapolation method of Campbell and Maffei (1970).The latter are generally in good agreement with each other. Whether this is a peculiarity of the swept-contrast technique, or is due to the much higher luminance employed (see Figure 4) remains to be clarified. I t is noteworthy, however, that peak contrast sensitivity at low photopic luminance (around 10 a t 10 weeks, according to most published data) deviates from the square-root law, in contrast with the contrast sensitivities found at low mesopic and high photopic luminances, which stand approximately in the same ratio a s the square-root of the respective luminances. One may speculate that contrast sensitivity results from the combined activity of different neuronal populations with different sensitivities, and that different experiments may reveal preferentially the contribution of one or the other of these populations. In summary, the data on infant CSF suggest that the M system. considered to be responsible for contrast detection of temporally modulated patterns of low spatial frequency, develops early, possibly during the first few months of life. This may appear difficult to reconcile with the fact that in the monkey, cells of the magnocellular LGN layers have to undergo a greater increase in contrast sensitivity during development than the cells of the parvocellular layers (Blakemore and Hawken. 1985). On the other hand, anatomical data on the plasticity of segregation of monocular inputs to the monkey striate cortex indicate that the postnatal period in which plastic changes can be induced in layer IVC. by reversal of monocular deprivation, is shorter

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for the magnocellular inputs to layer IVC-alpha t h a n for the parvocellular inputs to layer IVC-beta (LeVay et al., 1980). This is consistent with a shorter developmental period of the magnocellular, compared with the parvocellular pathway. Visual acuity takes much longer to develop fully than contrast sensitivity a t lower spatial frequencies and the major constraint to infant visual acuity is probably the immaturity of the retina, and in particular the fovea. Whether a t each age the resulting acuity reflects primarily the properties of the P system, as seems to be the case for the adult monkey, or whether the M system also contributes to spatial resolution in infancy requires further investigation. The visual functions considered so far define the lowest values of the luminance- and color-contrast, in the spatial and temporal frequency domain, below which no vision is possible. Probably these threshold characteristics result from constraints imposed already at the input to the visual cortex and/or a t the earliest stages of cortical processing. Further processing however is required for the perception of suprathreshold stimuli and for guiding visuomotor responses. Various visual functions reviewed in the previous sections imply cortical processing, e.g. orientation discrimination, motion perception, stereopsis and, possibly in part, vernier acuity. Orientation discrimination, at least in a crude form, is present at birth and rapidly becomes more selective. Discrimination of moving from stationary patterns, VEP responses to reversal of motion direction, and smooth oculomotor pursuit have a later onset. In the monkey, processing of motion information relevant both for the perception of moving objects and the control of smooth pursuit seems to proceed primarily along the cortical stream leading from V1 to MT (Newsome et al., 1985; Livingstone and Hubel, 1988; Newsome and Pare', 1988: Schiller et al., 1990). which receives its major input from the M pathway. Accordingly, one might interpret the onset of motion responses during the third and fourth month of life as a sign of the emergence of cortical activity along this route. Orientation and color information required for the perception of other stimulus attributes are likely to be processed primarily along the cortical stream from V1 through V2 and V4 to IT (Mishkin et al.. 1983; Livingstone and Hubel, 1988; Merigan, 1989; Schiller et al.. 1990). The early presence of orientation selectivity and of color discrimination in infants might indicate an early functionality of this route, but we do not know how long it will take for it to reach its full potential. There may be various developmental stages, a s suggested by the fact that the orientation and spatial frequency channels, that provide the basic machinery for a multiscale analysis of form, are present shortly after birth, while more complex stimulus interactions emerge later. Judging from the latest findings on stereo- and vernier-acuity in children, the development of some cortical processes may cover a period of several years. outlasting the maturation of more peripheral stages. In conclusion, there are indications that visual development proceeds at different rates and/or emerges a t different ages for visual functions that are likely to be mediated by different neural streams between the retina and the primary visual cortex. As to the functions that imply further cortical processing, we are just beginning to acquire some knowledge of their age of onset and duration of development.

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Although there are indications that these may differ for different visual capacities, an interpretation in terms of different intracortical pathways must await future research.

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