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Postnatal Development of Function in the Mammalian Visual System

Donald E. Mitchell, Brian Timney

10.1002/cphy.cp010312

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Development of Visual Perception
1.1 Methods of Study
1.2 Development of Spatial Resolution
1.3 Development of Depth Perception and Stereopsis
1.4 Overview
2 Development of Visual Neural Processes
2.1 Retina
2.2 Lateral Geniculate Nucleus
2.3 Visual Cortex
3 Consequences of Binocular Visual Deprivation
3.1 Forms of Binocular Deprivation
3.2 Effects on Perception
4 Effects of Selected Visual Experience on Neural Processes and Perception
5 Conditions that Influence Ocular Dominance
5.1 Monocular Deprivation
5.2 Artificial Strabismus
5.3 Alternating Monocular Deprivation
6 Conditions that Influence Other Receptive‐Field Properties
6.1 Orientation Selectivity
6.2 Movement and Direction Selectivity
6.3 Effects of Unusual Visual Input on Cortical Development
7 Genetic and Experiential Factors in Visual Development
7.1 Functional Role of Visual Experience
Figure 1. Figure 1.

Development of visual acuity in human infants. Data gathered using the preferential‐looking (PL) procedure. Targets were high‐contrast square‐wave gratings matched with homogeneous gray fields of same space‐averaged luminance.

Adapted from Gwiazda et al. 157. Copyright © 1982 American Academy of Optometry
Figure 2. Figure 2.

Contrast sensitivity functions of human infants at 1, ▴; 2, ▪; and 3, • mo of age. Data gathered by PL procedure for large sine‐wave gratings. Data for adults, ⋄, were obtained on same apparatus.

Adapted from Banks and Salapatek 18. Copyright 1978 by The C. V. Mosby Company, St. Louis, MO
Figure 3. Figure 3.

Development of visual acuity for square‐wave gratings for a single Macaca nemestrina monkey. Data obtained using PL procedure.

Adapted from Teller et al. 367. Copyright © 1978, with permission from Pergamon Press, Ltd
Figure 4. Figure 4.

Contrast sensitivity functions measured on 3 infant monkeys (Macaca nemestrina) at ages shown, in weeks, beside each curve. Data obtained by PL procedure.

From Boothe et al. 56. Copyright 1980 by the American Association for the Advancement of Science
Figure 5. Figure 5.

Development of visual acuity for square‐wave gratings in kittens obtained on jumping stand 248. Various symbols denote measurements made on different animals.

From Giffin and Mitchell 146
Figure 6. Figure 6.

Development of stereopsis in human infants. Data gathered using PL procedure. Infants sat 60 cm from 2 rear projection screens onto which 2 sets of stimuli were presented. Both sets of stimuli comprised 3 vertical bars 2° wide and spaced 2° apart. By means of polarizing filters in projectors and in lightweight goggles worn by infants, 1 set of stimuli was imaged with zero disparity and so appeared as 3 bars coplanar with screen, whereas on other screen the 2 outside bars were imaged with a known binocular disparity to appear (to a normal adult) as lying either in front of or behind central bar. Eight disparities ranging from 1 to 58 min of arc were tested. Data show smallest divergent disparities for which infants showed a preference on at least 80% of trials for 3 representative subjects of 16 examined.

Adapted from Held et al. 165
Figure 7. Figure 7.

Development of binocular depth perception in kittens measured using jumping stand 250. Data show threshold retinal disparity corresponding to smallest separation of target surfaces in depth that could be discriminated at various ages. Binocular disparity was calculated from knowledge of viewing distance and interocular separation. Each symbol represents data from different animal.

Adapted from Timney 371. Copyright 1981 by The C. V. Mosby Company, St. Louis, MO
Figure 8. Figure 8.

Optical quality of kitten eye compared with eye of adult cat. Calculated retinal contrasts [(Imax − Imin)/(Imax + Imin)] of 100% contrast square‐wave gratings imaged by eyes of 16‐ and 30‐day‐old kittens, and by eye of normal adult cat. Each data point represents contrast of retinal image computed from measurements of optical modulation transfer function at different ages. Latter functions derived from fundus photographs of retinal blood vessels.

From Bonds and Freeman 51. Copyright © 1978, with permission from Pergamon Press, Ltd
Figure 9. Figure 9.

Mean improvement in spatial resolution of foveal lateral geniculate nucleus (LGN) cells with age in normal and monocularly deprived monkeys. Each symbol depicts mean resolution of X‐cells with receptive fields located within 2° of central fovea. Recordings made in right LGN ipsilateral to deprived eye of monocularly occluded monkeys (stars). Filled circles depict resolution of cells driven by left eye; open circles plot comparable data from right eye. Data points from both eyes of individual animals joined by vertical line. Monocular deprivation was from day of birth until time of recording. Note that monocular deprivation does not hinder improvement in resolution with age, and that even in normal animals LGN cells driven by ipsilateral (right) eye possess slightly lower acuity than cells driven by contralateral eye.

From Blakemore and Vital‐Durand 45
Figure 10. Figure 10.

A: proportion of types of orientation selectivity within a population of visually responsive cells recorded from normal kittens at ages shown. Or., orientation selective; O.B., orientation biased; N.O., nonoriented. Number of visually responsive cells recorded in each age group shown on top. B: orientation specificity of orientation‐selective cells as function of age for both normal (filled circles) and dark‐reared (open circles) kittens. Ordinate indicates half width of tuning curve at half of maximum response. Bar represents ± 1 SEM, and numbers beside each symbol indicate number of cells studied at each age.

From Bonds 50
Figure 11. Figure 11.

Tuning of most selective binocular cortical cells to horizontal retinal disparity at various stages of development in kittens. Each circle indicates mean number of spikes (from 8–10 repetitions) elicited by movement of preferred stimulus over both receptive fields. Mean level of response elicited by monocular stimulation indicated by dotted horizontal lines. All cells were located within 5° of area centralis. Prior to 4th wk cells exhibited binocular facilitation that was relatively insensitive to changes in retinal disparity. Over course of next week zone of binocular facilitation became progressively narrower, and binocular response when receptive fields were not aligned fell below responses elicited monocularly.

From Pettigrew 293
Figure 12. Figure 12.

Development of visual acuity for square‐wave gratings for 4 cats that had been reared in total darkness from time of natural eye opening until either 4, 6, 8, or 10 mo of age indicated at top of graphs. During period indicated by horizontal line, animals were unable to perform pattern discriminations on jumping stand. Arrows indicate 1st day on which animals were able to discriminate an open from a closed door on jumping stand using visual cues alone.
Figure 13. Figure 13.

Comparison of effects of binocular deprivation with those of normal visual experience on development of various receptive‐field types in visual cortex of kittens. Open circles show percentages of each type of receptive field among sample of cells recorded from 7 normal kittens of different ages. Filled symbols show comparative data from 6 binocularly deprived kittens. In both cases curves originate from data from 9‐day‐old kitten recorded when eyelids were just beginning to part naturally. Data from animals deprived by bilateral lid suture are indicated by filled circles; those deprived by dark rearing are depicted by filled squares. Filled triangles show results from animals deprived by bilateral suture of nictitating membrane. Numbers beneath data points for top set of curves indicate total number of cells recorded in each animal.

From Blakemore and Van Sluyters 43
Figure 14. Figure 14.

Ocular dominance histograms for A: 223 cells recorded from visual cortex of a number of normal adult cats; B: 199 cells recorded from visual cortex of 5 kittens monocularly deprived by eyelid suture from time of natural eye opening until recording at between 8 and 14 wk of age; C: 26 cells recorded from single adult cat deprived by eyelid suture for 3 mo. In B and C, recordings were made from hemisphere contralateral to monocularly deprived eye. Cells are classified into 7 subjective ocular dominance groups according to relative influence of each of the 2 eyes. Cells classified as group 1 or 7 are excited exclusively by visual stimuli presented to eye contralateral or ipsilateral to recording electrode, respectively. Remaining groups are binocular; those classified as group 4 are influenced equally by the 2 eyes. Cells classified as belonging to groups 3 and 2 show progressively greater bias toward contralateral eye, whereas those classified as groups 5 and 6 exhibit increasing bias toward ipsilateral eye. Cells visually unresponsive denoted by letters VU (B). Letters C and I in A indicate groups dominated by contralateral and ipsilateral eye, respectively. Letters D and N in B and C beneath histograms denote ocular dominance group dominated by deprived and nondeprived eye, respectively.

Adapted from Hubel and Wiesel 186, and Wiesel and Hubel 416,417
Figure 15. Figure 15.

Autoradiographic montages showing labeling pattern of ocular dominance columns of layer IVc of normal (A and B) and monocularly deprived (C) monkeys (Macaca mulatta). A: pattern of labeling in hemisphere contralateral to injected eye of normal adult monkey. B: labeling pattern from 6‐wk‐old normal monkey ipsilateral to injected eye. Labeled bands are as distinct as in adults. C: labeling pattern from monkey whose right eye was closed by eyelid suture at 2 wk of age. Left eye injected when animal was 18 mo old. Note expansion of labeled columns from open eye at expense of unlabeled columns for deprived eye. However, periodicity of columns, about 750 μm for a left‐right pair, was identical to that of normal monkey. Unlabeled horizontal bars are 1 mm long.

From Hubel and Weisel 189 and LeVay et al. 229
Figure 16. Figure 16.

Behavioral recovery of visual acuity (for square‐wave gratings) of deprived eye of 4 cats monocularly deprived by eyelid suture from time of natural opening until ages indicated. After termination of period of monocular occlusion, visual input was allowed to both eyes. Measurement of visual acuity of formerly deprived eye was made with large opaque contact lens occluder covering nondeprived eye. During period indicated by horizontal lines animals were unable to make pattern discriminations on jumping stand. Arrows indicate days on which animals showed ability to discriminate a closed versus an open door on jumping stand using visual cues alone.

Data in A and B adapted from Giffin and Mitchell 146
Figure 17. Figure 17.

A‐K: ocular dominance distribution of sample of visual cortical neurons recorded in each of 11 kittens subjected to 10 and 12 days of monocular deprivation at progressively later ages. L: distribution of cortical ocular dominance of 4 normal kittens recorded at 45, 48, 55, or 135 days of age, respectively, is shown for comparison. Periods over which kittens (A‐K) were monocularly deprived were: A, 8–19 days; B, 18–27 days; C, 28–37 days; D, 38–47 days; E, 48–57 days; F, 58–67 days; G, 69–79 days; H, 80–90 days; I, 91–100 days; J, 99–109 days; K, 109–120 days. Right eye was deprived by eyelid suture in every case, and recordings were made in left (contralateral) hemisphere. Ocular dominance groups are as defined in Fig. 14.

From Olson and Freeman 277
Figure 18. Figure 18.

Profile of sensitive period for monocular deprivation in kittens. Filled circles depict degree of functional disconnection resulting from 10–12 days of monocular deprivation imposed on various kittens at ages indicated. Effect of deprivation period expressed by index based on proportion of cells dominated by ipsilateral (nondeprived) eye [(percentage of cells in groups 5–7) − N]/[100% − N.], where N was average percentage of cells in groups 5–7 (36%) in 4 normal kittens (see Fig. 17L). Open circles show data of Blakemore and Van Sluyters 32 obtained from kittens reverse sutured for 9 wk at ages indicated. Again, effect of period of reverse suture is expressed by index equal to proportion of cells dominated by originally deprived eye (percentage of cells in groups 5–7).

From Olson and Freeman 277
Figure 19. Figure 19.

Distribution of ocular dominance among samples of cells recorded from visual cortex of a number of cats monocularly deprived for 3 mo at ages indicated. In each case microelectrode was located in hemisphere contralateral to deprived eye.

From Cynader, Timney, and Mitchell 94
Figure 20. Figure 20.

Distribution of ocular dominance among sample of visual cortical cells recorded in each of 6 monkeys subjected to a period of monocular deprivation at progressively later ages. Periods of eyelid closure were from A, day 2 to day 24; B, day 21 to day 36; C, 5.5 wk to 16 mo; D, 10 wk to 16 mo; E, 1 yr to 2 yr; and F, 6 yr to 7.5 yr. Although effects of period of monocular deprivation were assessed only in right hemisphere of 3 monkeys (C, D, and F), results from these particular animals are depicted as if obtained from left hemisphere, contralateral to deprived eye. Ocular dominance groups are as defined for Fig. 14. Letter D indicates group completely dominated by the deprived eye.

Adapted from LeVay et al. 229
Figure 21. Figure 21.

Profile of sensitive period of visual cortex of monkeys to anatomical and physiological effects of monocular deprivation. Filled circles show effects of periods of monocular deprivation on cortical ocular dominance in cortical layers other than IVc (left ordinate), whereas open and filled squares depict concurrent effects on ocular dominance column area within layer IVc (right ordinate). Each filled circle depicts results from individual monkeys monocularly deprived at various ages for a duration indicated by length of horizontal line to right of each symbol. Physiological effects of period of monocular occlusion are expressed in form of normalized deprivation index calculated as follows: mean ocular dominance was first calculated from distribution of ocular dominance for sample of cortical cells recorded from each animal (such as those shown in Fig. 20). This was then normalized with respect to mean ocular dominance for normal animals 419 of 4.3 by using the formula (4.3 − mean ocular dominance)/3.3 for animals in which recordings were made in right hemisphere ipsilateral to deprived eye and the formula (mean ocular dominance −4.3)/2.7 for animals in which recordings were made in left hemisphere. Filled and open squares show effects of monocular deprivation on ocular dominance column area in layer IVc expressed as ratio L − R/L + R, where L and R denote area in layer IVc devoted to left (nondeprived) and right (deprived) eye, respectively. Filled symbols indicate effects on column area in left hemisphere contralateral to deprived eye, and open symbols show effect in right hemisphere.

Adapted from LeVay et al. 229
Figure 22. Figure 22.

Visual acuity of 23 human subjects with unilateral cataract (usually traumatic) immediately following restoration of normal visual input on removal of crystalline lens. Each subject is represented by a horizontal bar, whose length spans period of monocular deprivation and whose position with respect to ordinate defines first visual acuity score measured on careful optical correction following surgical removal of lens. Ordinate shows decimal acuity score where score of 1.0 represents an acuity of 6/6, and score of 0.1 is equivalent to 6/60. Subjects able to perceive only absence or presence of light (light perception) are designated by LP.

Adapted from Vaegan and Taylor 381
Figure 23. Figure 23.

Comparison of effects of 3‐mo monocular deprivation on distribution of ocular dominance in visual cortex of light‐reared or dark‐reared animals of same age. Ocular dominance groups are as defined for Fig. 14. Letter D indicates ocular dominance group completely dominated by deprived eye. In every case the recording electrode was located in hemisphere contralateral to monocularly deprived eye.

Adapted from Cynader and Mitchell 92
Figure 24. Figure 24.

Comparison of effects of optically and surgically induced strabismus on distribution of ocular dominance of cells in visual cortex. A, B: ocular dominance histograms from 2 kittens subjected to surgical (divergent) strabismus at 4 wk of age, then kept in darkness except for a period of visual exposure of 1 h each day until recording at 6 wk of age. C, D: histograms obtained from 2 kittens fitted with goggles that contained a total of 10Δ of vertical prism (5Δ base‐up in front of right eye and 5Δ base‐down before left eye) at 4 wk of age. As with other pair of kittens, animals received 1 h of exposure each day; at all other times they were kept in total darkness until recording at 6 wk of age. E: control data from normal kitten allowed visual experience for only 1 h each day from 4 wk of age until date of recording at 6 wk of age.

From Van Sluyters and Levitt 387
Figure 25. Figure 25.

Polar histograms of preferred orientations for samples of orientation‐specific cortical cells recorded from 2 kittens reared with monocular visual exposure to contours of a single orientation, analyzed by method described in text. Receptive fields were plotted with a Dove prism before the eye that was rotated a variable, but known, angle between each cell. Preferred orientations plotted here are corrected for setting of prism. Solid arrows indicate contour orientation to which kittens were exposed, horizontal for K330 and vertical for K370.

Adapted from Blakemore 33
Figure 26. Figure 26.

Effects of different degrees of astigmatism on appearance of a target, A, consisting of a radiating series of lines of different orientations. When axes of the astigmatism are horizontal and vertical, as shown, contours parallel to focal line imaged in film plane (vertical) are imaged clearly, whereas contours of other orientations become progressively more blurred toward horizontal.
Figure 27. Figure 27.

Contrast sensitivity functions for gratings of various orientations measured A: on normal adult human; B: on optically corrected adult astigmat with meridional amblyopia, whose early visual input was similar to that depicted in Fig. 26; and C: for left eye of a rhesus monkey (Macaca mulatta) with oblique axis astigmatism that was optically corrected for these measurements. In A, filled and open symbols indicate results obtained with vertical horizontal gratings, respectively. Similar symbols in B depict contrast sensitivities for gratings that were nearly vertical and horizontal (75° and 165°) close to axes of astigmatism. Filled and open triangles in C indicate contrast sensitivities for gratings oriented at 45° and 135°, respectively. In contrast to normal humans, A, astigmat in B resolved vertical gratings far better than horizontal gratings, even though optical astigmatism was fully corrected. Similarly, astigmatic monkey, C, exhibited equally large differences in resolution between gratings at 45° and 135°, again in marked contrast to results from normal monkeys 149, which resolve gratings of these two orientations equally well. Astigmatic errors were B: −0.25D spherical error; cylindrical error −4.50D axis 20°; C: L + 1.25D spherical error; cylindrical error −1.00D axis 45°.

Adapted from Mitchell and Wilkinson 253 and Harwerth et al. 162
Figure 28. Figure 28.

Tuning of 3 binocular cells recorded in visual Wulst of an adult barn owl (Tyto alba) for horizontal retinal disparity. Recordings were made simultaneously from both right and left visual Wulst. Unit B8, recorded from right visual Wulst, served as a reference cell that was held for some time while first unit A4 and then A10 were investigated in left visual Wulst. Connected symbols show response of each cell to a vertical slit swept across 2 receptive fields. Data points to right indicate response of each cell to monocular presentations of stimulus (R, right eye; L, left eye). Connected symbols show response of each cell to binocular stimulation as a function of changes in horizontal retinal disparity produced by alterations of setting of a variable‐power (Risley) prism mounted in front of left eye. Because visual axes are divergent under paralysis, each cell gives its best response with convergent setting of prism. Nevertheless each cell exhibits clear preference for a different retinal disparity.

From Pettigrew and Konishi 300. Copyright 1976 by the American Association for the Advancement of Science
Figure 29. Figure 29.

Ocular dominance histograms for cells recorded from visual Wulst of A: normal barn owls (Tyto alba); and B: 2 owlets subjected to monocular deprivation by eyelid suture for 2–3 mo from postnatal day 11 or 29. In all cases microelectrode was located in left hemisphere, which for monocularly deprived owlets was contralateral to deprived eye. Ocular dominance groups are as for cats in Fig. 14. Group 4 cells in filled portion of histogram in A could be driven only by simultaneous presentation of stimuli to both eyes at a certain precise binocular disparity and could not be excited at all monocularly. Cells unresponsive to visual stimulation are indicated by U.

From Pettigrew and Konishi 299; reprinted by permission from Nature 264: 753–754, 1976. Copyright © 1976 Macmillan Journals Limited


Figure 1.

Development of visual acuity in human infants. Data gathered using the preferential‐looking (PL) procedure. Targets were high‐contrast square‐wave gratings matched with homogeneous gray fields of same space‐averaged luminance.

Adapted from Gwiazda et al. 157. Copyright © 1982 American Academy of Optometry


Figure 2.

Contrast sensitivity functions of human infants at 1, ▴; 2, ▪; and 3, • mo of age. Data gathered by PL procedure for large sine‐wave gratings. Data for adults, ⋄, were obtained on same apparatus.

Adapted from Banks and Salapatek 18. Copyright 1978 by The C. V. Mosby Company, St. Louis, MO


Figure 3.

Development of visual acuity for square‐wave gratings for a single Macaca nemestrina monkey. Data obtained using PL procedure.

Adapted from Teller et al. 367. Copyright © 1978, with permission from Pergamon Press, Ltd


Figure 4.

Contrast sensitivity functions measured on 3 infant monkeys (Macaca nemestrina) at ages shown, in weeks, beside each curve. Data obtained by PL procedure.

From Boothe et al. 56. Copyright 1980 by the American Association for the Advancement of Science


Figure 5.

Development of visual acuity for square‐wave gratings in kittens obtained on jumping stand 248. Various symbols denote measurements made on different animals.

From Giffin and Mitchell 146


Figure 6.

Development of stereopsis in human infants. Data gathered using PL procedure. Infants sat 60 cm from 2 rear projection screens onto which 2 sets of stimuli were presented. Both sets of stimuli comprised 3 vertical bars 2° wide and spaced 2° apart. By means of polarizing filters in projectors and in lightweight goggles worn by infants, 1 set of stimuli was imaged with zero disparity and so appeared as 3 bars coplanar with screen, whereas on other screen the 2 outside bars were imaged with a known binocular disparity to appear (to a normal adult) as lying either in front of or behind central bar. Eight disparities ranging from 1 to 58 min of arc were tested. Data show smallest divergent disparities for which infants showed a preference on at least 80% of trials for 3 representative subjects of 16 examined.

Adapted from Held et al. 165


Figure 7.

Development of binocular depth perception in kittens measured using jumping stand 250. Data show threshold retinal disparity corresponding to smallest separation of target surfaces in depth that could be discriminated at various ages. Binocular disparity was calculated from knowledge of viewing distance and interocular separation. Each symbol represents data from different animal.

Adapted from Timney 371. Copyright 1981 by The C. V. Mosby Company, St. Louis, MO


Figure 8.

Optical quality of kitten eye compared with eye of adult cat. Calculated retinal contrasts [(Imax − Imin)/(Imax + Imin)] of 100% contrast square‐wave gratings imaged by eyes of 16‐ and 30‐day‐old kittens, and by eye of normal adult cat. Each data point represents contrast of retinal image computed from measurements of optical modulation transfer function at different ages. Latter functions derived from fundus photographs of retinal blood vessels.

From Bonds and Freeman 51. Copyright © 1978, with permission from Pergamon Press, Ltd


Figure 9.

Mean improvement in spatial resolution of foveal lateral geniculate nucleus (LGN) cells with age in normal and monocularly deprived monkeys. Each symbol depicts mean resolution of X‐cells with receptive fields located within 2° of central fovea. Recordings made in right LGN ipsilateral to deprived eye of monocularly occluded monkeys (stars). Filled circles depict resolution of cells driven by left eye; open circles plot comparable data from right eye. Data points from both eyes of individual animals joined by vertical line. Monocular deprivation was from day of birth until time of recording. Note that monocular deprivation does not hinder improvement in resolution with age, and that even in normal animals LGN cells driven by ipsilateral (right) eye possess slightly lower acuity than cells driven by contralateral eye.

From Blakemore and Vital‐Durand 45


Figure 10.

A: proportion of types of orientation selectivity within a population of visually responsive cells recorded from normal kittens at ages shown. Or., orientation selective; O.B., orientation biased; N.O., nonoriented. Number of visually responsive cells recorded in each age group shown on top. B: orientation specificity of orientation‐selective cells as function of age for both normal (filled circles) and dark‐reared (open circles) kittens. Ordinate indicates half width of tuning curve at half of maximum response. Bar represents ± 1 SEM, and numbers beside each symbol indicate number of cells studied at each age.

From Bonds 50


Figure 11.

Tuning of most selective binocular cortical cells to horizontal retinal disparity at various stages of development in kittens. Each circle indicates mean number of spikes (from 8–10 repetitions) elicited by movement of preferred stimulus over both receptive fields. Mean level of response elicited by monocular stimulation indicated by dotted horizontal lines. All cells were located within 5° of area centralis. Prior to 4th wk cells exhibited binocular facilitation that was relatively insensitive to changes in retinal disparity. Over course of next week zone of binocular facilitation became progressively narrower, and binocular response when receptive fields were not aligned fell below responses elicited monocularly.

From Pettigrew 293


Figure 12.

Development of visual acuity for square‐wave gratings for 4 cats that had been reared in total darkness from time of natural eye opening until either 4, 6, 8, or 10 mo of age indicated at top of graphs. During period indicated by horizontal line, animals were unable to perform pattern discriminations on jumping stand. Arrows indicate 1st day on which animals were able to discriminate an open from a closed door on jumping stand using visual cues alone.



Figure 13.

Comparison of effects of binocular deprivation with those of normal visual experience on development of various receptive‐field types in visual cortex of kittens. Open circles show percentages of each type of receptive field among sample of cells recorded from 7 normal kittens of different ages. Filled symbols show comparative data from 6 binocularly deprived kittens. In both cases curves originate from data from 9‐day‐old kitten recorded when eyelids were just beginning to part naturally. Data from animals deprived by bilateral lid suture are indicated by filled circles; those deprived by dark rearing are depicted by filled squares. Filled triangles show results from animals deprived by bilateral suture of nictitating membrane. Numbers beneath data points for top set of curves indicate total number of cells recorded in each animal.

From Blakemore and Van Sluyters 43


Figure 14.

Ocular dominance histograms for A: 223 cells recorded from visual cortex of a number of normal adult cats; B: 199 cells recorded from visual cortex of 5 kittens monocularly deprived by eyelid suture from time of natural eye opening until recording at between 8 and 14 wk of age; C: 26 cells recorded from single adult cat deprived by eyelid suture for 3 mo. In B and C, recordings were made from hemisphere contralateral to monocularly deprived eye. Cells are classified into 7 subjective ocular dominance groups according to relative influence of each of the 2 eyes. Cells classified as group 1 or 7 are excited exclusively by visual stimuli presented to eye contralateral or ipsilateral to recording electrode, respectively. Remaining groups are binocular; those classified as group 4 are influenced equally by the 2 eyes. Cells classified as belonging to groups 3 and 2 show progressively greater bias toward contralateral eye, whereas those classified as groups 5 and 6 exhibit increasing bias toward ipsilateral eye. Cells visually unresponsive denoted by letters VU (B). Letters C and I in A indicate groups dominated by contralateral and ipsilateral eye, respectively. Letters D and N in B and C beneath histograms denote ocular dominance group dominated by deprived and nondeprived eye, respectively.

Adapted from Hubel and Wiesel 186, and Wiesel and Hubel 416,417


Figure 15.

Autoradiographic montages showing labeling pattern of ocular dominance columns of layer IVc of normal (A and B) and monocularly deprived (C) monkeys (Macaca mulatta). A: pattern of labeling in hemisphere contralateral to injected eye of normal adult monkey. B: labeling pattern from 6‐wk‐old normal monkey ipsilateral to injected eye. Labeled bands are as distinct as in adults. C: labeling pattern from monkey whose right eye was closed by eyelid suture at 2 wk of age. Left eye injected when animal was 18 mo old. Note expansion of labeled columns from open eye at expense of unlabeled columns for deprived eye. However, periodicity of columns, about 750 μm for a left‐right pair, was identical to that of normal monkey. Unlabeled horizontal bars are 1 mm long.

From Hubel and Weisel 189 and LeVay et al. 229


Figure 16.

Behavioral recovery of visual acuity (for square‐wave gratings) of deprived eye of 4 cats monocularly deprived by eyelid suture from time of natural opening until ages indicated. After termination of period of monocular occlusion, visual input was allowed to both eyes. Measurement of visual acuity of formerly deprived eye was made with large opaque contact lens occluder covering nondeprived eye. During period indicated by horizontal lines animals were unable to make pattern discriminations on jumping stand. Arrows indicate days on which animals showed ability to discriminate a closed versus an open door on jumping stand using visual cues alone.

Data in A and B adapted from Giffin and Mitchell 146


Figure 17.

A‐K: ocular dominance distribution of sample of visual cortical neurons recorded in each of 11 kittens subjected to 10 and 12 days of monocular deprivation at progressively later ages. L: distribution of cortical ocular dominance of 4 normal kittens recorded at 45, 48, 55, or 135 days of age, respectively, is shown for comparison. Periods over which kittens (A‐K) were monocularly deprived were: A, 8–19 days; B, 18–27 days; C, 28–37 days; D, 38–47 days; E, 48–57 days; F, 58–67 days; G, 69–79 days; H, 80–90 days; I, 91–100 days; J, 99–109 days; K, 109–120 days. Right eye was deprived by eyelid suture in every case, and recordings were made in left (contralateral) hemisphere. Ocular dominance groups are as defined in Fig. 14.

From Olson and Freeman 277


Figure 18.

Profile of sensitive period for monocular deprivation in kittens. Filled circles depict degree of functional disconnection resulting from 10–12 days of monocular deprivation imposed on various kittens at ages indicated. Effect of deprivation period expressed by index based on proportion of cells dominated by ipsilateral (nondeprived) eye [(percentage of cells in groups 5–7) − N]/[100% − N.], where N was average percentage of cells in groups 5–7 (36%) in 4 normal kittens (see Fig. 17L). Open circles show data of Blakemore and Van Sluyters 32 obtained from kittens reverse sutured for 9 wk at ages indicated. Again, effect of period of reverse suture is expressed by index equal to proportion of cells dominated by originally deprived eye (percentage of cells in groups 5–7).

From Olson and Freeman 277


Figure 19.

Distribution of ocular dominance among samples of cells recorded from visual cortex of a number of cats monocularly deprived for 3 mo at ages indicated. In each case microelectrode was located in hemisphere contralateral to deprived eye.

From Cynader, Timney, and Mitchell 94


Figure 20.

Distribution of ocular dominance among sample of visual cortical cells recorded in each of 6 monkeys subjected to a period of monocular deprivation at progressively later ages. Periods of eyelid closure were from A, day 2 to day 24; B, day 21 to day 36; C, 5.5 wk to 16 mo; D, 10 wk to 16 mo; E, 1 yr to 2 yr; and F, 6 yr to 7.5 yr. Although effects of period of monocular deprivation were assessed only in right hemisphere of 3 monkeys (C, D, and F), results from these particular animals are depicted as if obtained from left hemisphere, contralateral to deprived eye. Ocular dominance groups are as defined for Fig. 14. Letter D indicates group completely dominated by the deprived eye.

Adapted from LeVay et al. 229


Figure 21.

Profile of sensitive period of visual cortex of monkeys to anatomical and physiological effects of monocular deprivation. Filled circles show effects of periods of monocular deprivation on cortical ocular dominance in cortical layers other than IVc (left ordinate), whereas open and filled squares depict concurrent effects on ocular dominance column area within layer IVc (right ordinate). Each filled circle depicts results from individual monkeys monocularly deprived at various ages for a duration indicated by length of horizontal line to right of each symbol. Physiological effects of period of monocular occlusion are expressed in form of normalized deprivation index calculated as follows: mean ocular dominance was first calculated from distribution of ocular dominance for sample of cortical cells recorded from each animal (such as those shown in Fig. 20). This was then normalized with respect to mean ocular dominance for normal animals 419 of 4.3 by using the formula (4.3 − mean ocular dominance)/3.3 for animals in which recordings were made in right hemisphere ipsilateral to deprived eye and the formula (mean ocular dominance −4.3)/2.7 for animals in which recordings were made in left hemisphere. Filled and open squares show effects of monocular deprivation on ocular dominance column area in layer IVc expressed as ratio L − R/L + R, where L and R denote area in layer IVc devoted to left (nondeprived) and right (deprived) eye, respectively. Filled symbols indicate effects on column area in left hemisphere contralateral to deprived eye, and open symbols show effect in right hemisphere.

Adapted from LeVay et al. 229


Figure 22.

Visual acuity of 23 human subjects with unilateral cataract (usually traumatic) immediately following restoration of normal visual input on removal of crystalline lens. Each subject is represented by a horizontal bar, whose length spans period of monocular deprivation and whose position with respect to ordinate defines first visual acuity score measured on careful optical correction following surgical removal of lens. Ordinate shows decimal acuity score where score of 1.0 represents an acuity of 6/6, and score of 0.1 is equivalent to 6/60. Subjects able to perceive only absence or presence of light (light perception) are designated by LP.

Adapted from Vaegan and Taylor 381


Figure 23.

Comparison of effects of 3‐mo monocular deprivation on distribution of ocular dominance in visual cortex of light‐reared or dark‐reared animals of same age. Ocular dominance groups are as defined for Fig. 14. Letter D indicates ocular dominance group completely dominated by deprived eye. In every case the recording electrode was located in hemisphere contralateral to monocularly deprived eye.

Adapted from Cynader and Mitchell 92


Figure 24.

Comparison of effects of optically and surgically induced strabismus on distribution of ocular dominance of cells in visual cortex. A, B: ocular dominance histograms from 2 kittens subjected to surgical (divergent) strabismus at 4 wk of age, then kept in darkness except for a period of visual exposure of 1 h each day until recording at 6 wk of age. C, D: histograms obtained from 2 kittens fitted with goggles that contained a total of 10Δ of vertical prism (5Δ base‐up in front of right eye and 5Δ base‐down before left eye) at 4 wk of age. As with other pair of kittens, animals received 1 h of exposure each day; at all other times they were kept in total darkness until recording at 6 wk of age. E: control data from normal kitten allowed visual experience for only 1 h each day from 4 wk of age until date of recording at 6 wk of age.

From Van Sluyters and Levitt 387


Figure 25.

Polar histograms of preferred orientations for samples of orientation‐specific cortical cells recorded from 2 kittens reared with monocular visual exposure to contours of a single orientation, analyzed by method described in text. Receptive fields were plotted with a Dove prism before the eye that was rotated a variable, but known, angle between each cell. Preferred orientations plotted here are corrected for setting of prism. Solid arrows indicate contour orientation to which kittens were exposed, horizontal for K330 and vertical for K370.

Adapted from Blakemore 33


Figure 26.

Effects of different degrees of astigmatism on appearance of a target, A, consisting of a radiating series of lines of different orientations. When axes of the astigmatism are horizontal and vertical, as shown, contours parallel to focal line imaged in film plane (vertical) are imaged clearly, whereas contours of other orientations become progressively more blurred toward horizontal.



Figure 27.

Contrast sensitivity functions for gratings of various orientations measured A: on normal adult human; B: on optically corrected adult astigmat with meridional amblyopia, whose early visual input was similar to that depicted in Fig. 26; and C: for left eye of a rhesus monkey (Macaca mulatta) with oblique axis astigmatism that was optically corrected for these measurements. In A, filled and open symbols indicate results obtained with vertical horizontal gratings, respectively. Similar symbols in B depict contrast sensitivities for gratings that were nearly vertical and horizontal (75° and 165°) close to axes of astigmatism. Filled and open triangles in C indicate contrast sensitivities for gratings oriented at 45° and 135°, respectively. In contrast to normal humans, A, astigmat in B resolved vertical gratings far better than horizontal gratings, even though optical astigmatism was fully corrected. Similarly, astigmatic monkey, C, exhibited equally large differences in resolution between gratings at 45° and 135°, again in marked contrast to results from normal monkeys 149, which resolve gratings of these two orientations equally well. Astigmatic errors were B: −0.25D spherical error; cylindrical error −4.50D axis 20°; C: L + 1.25D spherical error; cylindrical error −1.00D axis 45°.

Adapted from Mitchell and Wilkinson 253 and Harwerth et al. 162


Figure 28.

Tuning of 3 binocular cells recorded in visual Wulst of an adult barn owl (Tyto alba) for horizontal retinal disparity. Recordings were made simultaneously from both right and left visual Wulst. Unit B8, recorded from right visual Wulst, served as a reference cell that was held for some time while first unit A4 and then A10 were investigated in left visual Wulst. Connected symbols show response of each cell to a vertical slit swept across 2 receptive fields. Data points to right indicate response of each cell to monocular presentations of stimulus (R, right eye; L, left eye). Connected symbols show response of each cell to binocular stimulation as a function of changes in horizontal retinal disparity produced by alterations of setting of a variable‐power (Risley) prism mounted in front of left eye. Because visual axes are divergent under paralysis, each cell gives its best response with convergent setting of prism. Nevertheless each cell exhibits clear preference for a different retinal disparity.

From Pettigrew and Konishi 300. Copyright 1976 by the American Association for the Advancement of Science


Figure 29.

Ocular dominance histograms for cells recorded from visual Wulst of A: normal barn owls (Tyto alba); and B: 2 owlets subjected to monocular deprivation by eyelid suture for 2–3 mo from postnatal day 11 or 29. In all cases microelectrode was located in left hemisphere, which for monocularly deprived owlets was contralateral to deprived eye. Ocular dominance groups are as for cats in Fig. 14. Group 4 cells in filled portion of histogram in A could be driven only by simultaneous presentation of stimuli to both eyes at a certain precise binocular disparity and could not be excited at all monocularly. Cells unresponsive to visual stimulation are indicated by U.

From Pettigrew and Konishi 299; reprinted by permission from Nature 264: 753–754, 1976. Copyright © 1976 Macmillan Journals Limited
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Article Title: Postnatal Development of Function in the Mammalian Visual System
 

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Donald E. Mitchell, Brian Timney. Postnatal Development of Function in the Mammalian Visual System. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 507-555. First published in print 1984. doi: 10.1002/cphy.cp010312