Perceptual Development in infancy

The Minnesota Symposia on Child Psychology, Volume 20

A. Yonas

• Publisher: Psychology Press
• Year: 2013
• Print ISBN:
  9780805800104
• Edition: 1
• eBook ISBN:
  9781134733538
• Topic: Psychology
• Subtopic: Developmental Psychology
• Index: Psychology

Each year, the Institute of Child Development brings together a group of distinguished investigators who share a common desire to understand the nature of development. The chapters in this volume are based on papers presented at the 20th of this continuing series, the Minnesota Symposia on Child Psychology. The meetings were held October 31 through November 2, 1985, at the University of Minnesota.

1 The Recovery From Early Monocular Visual Deprivation in Kittens

Donald E. Mitchell

Psychology Department, Dalhousie University

There is little doubt that the immense current interest in visual development can be attributed to the tremendous impact of two of the early papers of Hubel and Wiesel (Hubel & Wiesel, 1963; Wiesel & Hubel, 1963) that were published only 1 year after their pioneering documentation of the functional characteristics of cells in the adult cat visual cortex (Hubel & Wiesel, 1962). In these next two papers, Hubel and Wiesel described the functional status of the neonatal kitten visual cortex prior to visual experience as well as some of the drastic consequences of early selective visual input on the functional properties of cortical cells. In so doing they pioneered experimental inquiry into the manner by which the visual response characteristics of cells in the adult visual cortex acquire their highly complex nature in early postnatal life. Hubel and Wiesel (1963) concluded that many of the visual response characteristics of cortical cells that they reported earlier in adult cats could also be recognized in the neonatal kitten cortex. Although there were very obvious differences between the status of the neonatal cortex and that of adults, Hubel and Wiesel were more impressed by the similarities between the two and concluded that certain functional characteristics of cortical cells were established crudely at birth under genetic instruction. However, the results of the second paper, which described the consequences of restricting patterned visual input to only one eye for several months, indicated that certain functional properties of cortical cells were also profoundly influenced by early visual experience.

In normally reared adult cats, and young kittens as well, most visual cortical cells (approx. 80%) can be excited by visual stimulation of either eye. There is a slight tendency for the contralateral eye to dominate in each hemisphere, but overall the two eyes influence the same proportion of cells (see Fig. 1.1 A). The situation is very different in kittens that have been deprived of pattern vision in one eye for several weeks in early postnatal life. Outside of layer IV virtually no cells in area 17 can be excited at all through the deprived eye. Two examples of the highly skewed nature of the ocular dominance distributions derived from cortical recordings made from two animals that were reported in Wiesel and Hubel's (1963) original paper are shown in Figs. 1.1B and 1.1C. The existence of a sensitive period for the physiological effects of monocular deprivation was also made evident in this early paper because the shifts of ocular dominance in favor of the nondeprived eye were less in kittens monocularly deprived at 9 weeks of age (Fig. 1.1C) than those deprived when only 1-week-old (Fig. 1.1B). In addition, an adult cat monocularly deprived for 3 months showed no obvious shift of ocular dominance toward the nondeprived eye (Fig. 1.1D). The later extensive work of Hubel and Wiesel as well as other workers (e.g., Blakemore & Van Sluyters, 1974; Cynader, Timney, & Mitchell, 1980; Hubel & Wiesel, 1970; LeVay, Hubel, & Wiesel, 1980; Olson & Freeman, 1980) that defined more accurately the period of susceptibility of the cat and monkey visual cortex to the physiological effects of monocular deprivation is discussed elsewhere (Mitchell, 1981; Mitchell & Timney, 1984) and is not described in detail here. However, without exaggeration it can be stated that documentation of the sensitive periods of the visual cortex to the physiological effects of monocular deprivation and other forms of selective visual deprivation represents one of the major accomplishments of the work on visual development that has ensued in the 20 years since publication of Wiesel and Hubel's (1963) original developmental paper. Since this paper, it has become apparent that the sensitive period to the effects of monocular deprivation for both cats and monkeys is shorter for layer IV of the visual cortex than for the other layers, and that there may be different sensitive periods for modifying other visual cortical areas (Jones, Spear, & Tong, 1984) and other aspects of neural functioning in the visual cortex, such as directional selectivity (Daw & Wyatt, 1976). Furthermore, there are clear indications that the duration of the sensitive period for modification of a particular neural function may not be solely dependent on age, but may also depend on the state of functional development. Thus, for example, there is evidence that the period of susceptibility to the physiological effects of monocular deprivation is extended in animals reared in total darkness (Cynader & Mitchell, 1980; Mower, Berry, Burchfiel, & Duffy, 1981) and that animals reared in stroboscopic illumination from birth for long periods retain a certain degree of cortical plasticity even as adults (Pasternak, Movshon, & Merrigan, 1981). More detailed summaries of this and other work on sensitive periods in visual development are available in a number of recent reviews (Mitchell & Timney, 1984; Movshon & Van Sluyters, 1981).

FIG. 1.1 Ocular dominance distributions for samples of cells recorded in the visual cortex of normal adult cats (A), and in a series of kittens (B–D) that were monocularly deprived from near birth until the time of recording. The histogram A shows results from a sample of 223 cells recorded from a number of normal adult cats. Ocular dominance groups in this and subsequent figures were defined according to the conventions of Hubel and Wiesel (1962). Cells classified as belonging to groups 1 and 7 could be excited by visual stimulation of only one eye, the eye that was, respectively, contralateral and ipsilateral to the recording electrode. Cells in group 2 were dominated strongly, and those in group 3 weakly, by the contralateral eye. Likewise, cells classified as group 6 were dominated strongly by the ipsilateral eye, whereas those in group 5 were only weakly dominated by that eye. Group 4 cells were excited equally by either eye. Cells labeled o were unresponsive to visual stimuli. The histograms B–D represent data from 3 deprived animals whose rearing histories were as follows: B, a kitten monocularly deprived by eyelid suture from day 8 to 2 1/2 months of age; C, a kitten monocularly deprived at 9 weeks until 4 months of age; and D, an adult cat that was monocularly deprived for 3 months. For the 3 deprived animals of B–D, the recording electrode was located in the visual cortex contralateral to the deprived eye. Data redrawn from Wiesel and Hubel (1963).

At first, the sensitive period was conceptualized only as a period of time during which functional neural connections could be modified by abnormal early visual input. However, in a very important study, Blakemore and Van Sluyters (1974) demonstrated the highly plastic nature of neural connections during the sensitive period by noting that it also represented a time during which abnormal functional neural development resulting from a very early period of selective visual deprivation could be partially or even completely reversed by subsequent visual exposure. Specifically, they established that the ocular dominance of cortical cells in monocularly deprived kittens could be switched from complete dominance by the nondeprived eye to dominance by the deprived eye if occlusion was reversed sufficiently early (5 weeks of age) in order to force the animal to use its formerly deprived eye.

The demonstration of the vulnerability of the visual cortex to environmental influences in general, as well as the emergence of the concept of sensitive periods in development in particular, has provided the motivation for much of the subsequent work on visual development. In most cases this work has been motivated by the desire to understand the rules that govern the way in which functional neural connections are established in the visual cortex and the extent to which they are influenced by early visual experience. However, somewhat less commonly there has been a quite different motive that stems from the close similarity between the visual impairments exhibited by monocularly deprived kittens or monkeys when using their deprived eye and the visual deficits reported in certain forms of human amblyopia. This interest has also been fostered by the demonstrations of the reversibility of the effects of early monocular visual deprivation that raise the possibility of both an ultimate understanding of the origins of amblyopia and the development of better methods of treatment.

Amblyopia is a commmon clinical condition characterized by a reduction of visual acuity in one or (less commonly) both eyes that cannot be attributed to disease or to an optical error. Because amblyopia is frequently found to be associated with anisometropia, strabismus, or other conditions that disturb the degree of concordance of the visual input to the two eyes, it has long been thought to result from an abnormality of development in the central visual pathways that is linked in some way to the early discordant binocular visual input. In one form of human amblyopia referred to as deprivation amblyopia (Von Noorden, 1967), there is an early severe impediment to clear imagery to one eye such as a cataract or corneal scarring that results in a degree of image degradation comparable to that which accompanies the experimental procedure of monocular eyelid suture. But in other forms of amblyopia, such as that associated with anisometropia (unequal refractive errors in the two eyes), the loss of image quality in one eye may be less. Nevertheless, it can be argued that study of the abnormal cortical development that occurs following various forms of early selected visual deprivation may provide insight into the origin(s) of the visual deficits observed in human amblyopia. Studies with this applied motive are by no means limited to experiments with visually deprived animals because it also represents a major theme in recent studies of visual develoment in human infants that chronicle the anomolous development associated with various naturally occurring impediments to normal binocular visual input (see also chapter 2) such as anisometropia and strabismus.

Similar considerations provided the major motive for much of my research on normal and abnormal development in kittens. My initial work in this area examined the consequences for vision of early restricted exposure to contours of a single orientation (Blasdel, Mitchell, Muir, & Pettigrew, 1977; Muir & Mitchell, 1973, 1975) but soon afterward my attention turned to studies of the more dramatic visual consequences of other forms of abnormal early visual exposure, such as monocular deprivation (Giffin & Mitchell, 1978; Mitchell, Giffin, & Timney, 1977). One of the very first studies I conducted on visually deprived kittens following development of the jumping stand procedure (Mitchell, Cynader, & Movshon, 1977; Mitchell, Giffin, Wilkinson, Anderson, & Smith, 1976) compared the extent and the time course of the behavioral recovery from various periods of monocular deprivation imposed from birth. The idea behind these studies was that they would provide a method for documenting the sensitive period of the visual system as a whole to the behavioral effects of monocular deprivation.

In addition to a preoccupation with fundamental questions concerning the nature of sensitive periods in visual development, I began to examine in detail the factors that were known to promote recovery from early monocular deprivation. Although by no means the only motive, I thought that such studies might help establish a more rational basis for the treatment of human amblyopia. For nearly 2 centuries (Duke-Elder & Wybar, 1971) the treatment of this condition has involved some form of patching therapy whereby the nonamblyopic eye is occluded by a patch for a period of weeks or months in order to force the amblyopic child to employ its poor eye. As attested to by its very longevity as the preferred treatment, this procedure can promote some improvement in the vision of the amblyopic eye in certain cases. However, the improvement is more often only very limited and even in cases where it does occur, the improvement in vision is often small and sometimes also temporary. From the time of Worth's classic work (Worth, 1903) on strabismus at the beginning of this century, it has been recognized that the treatment of this and other developmental visual disorders is more likely to be successful if initiated very early in life, a conclusion that presaged the discovery of sensitive periods in mammalian visual development. However, without firm knowledge of the time course of sensitive periods in human visual development, nor of the physiological mechanisms that underlie recovery from early visual deprivation, it is not surprising that treatment of amblyopia is only rarely successful. Nevertheless, the explosion of knowledge that has emerged in the last 10 years concerning normal and abnormal development in the mammalian visual system sets the stage for the eventual elucidation of more successful procedures for the treatment of human amblyopia.

A logical first step in this direction would be to examine procedures that optimize recovery from early forms of visual deprivation in kittens. Because of the large differences between the durations of the sensitive periods in visual development in cats and humans, it would be unlikely that the specific timing of procedures that optimize recovery in kittens could be applied directly to humans. Nevertheless, by reference to common landmarks in anatomical and physiological development in the visual pathways of cats, monkeys, and humans (such as the time of segregation of ocular dominance columns in layer IV of area 17) it should be possible to establish appropriate weighting factors from procedures developed for the cat, and later refined on monkeys, that would permit calculation of the appropriate treatment regimens for humans. Certainly this work on kittens could serve as a guide to the conduct of crucial experiments on monocularly deprived macaque monkeys that would in turn establish optimum treatment schedules for this species. Extrapolation from monkeys to humans is at present far simpler than from cats because rules of thumb for relating monkey and human ages in visual development have already been established (Boothe, Dobson, & Teller, 1985).

This chapter provides a summary of experiments conducted in the last 10 years that examine the recovery from monocular deprivation and that pertain to the issues just raised. In the view of the emerging interest in the anomolous development that occurs in human infants with abnormal early sensory input (e.g., Atkinson & Braddick, this volume; Maurer, Lewis, & Brent, in press), emphasis is placed on the more recent kitten studies that examine factors that promote recovery from the visual deficits induced by early monocular visual deprivation.

SENSITIVE PERIODS DEFINED BY RECOVERY FROM EARLY DEPRIVATION

Although the anatomical, physiological, and behavioral consequences of monocular deprivation are very severe, some recovery is possible if normal patterned visual input is restored to the deprived eye sufficiently early in life. As mentioned earlier, the degree of recovery can be enhanced if at the time that visual input is restored to the deprived eye, the other eye is occluded (reverse occlusion). However, even when the formerly...

Table of contents

• Front Cover
• Half Title
• Title Page
• Copyright
• Contents
• Preface
• 1. The Recovery From Early Monocular Visual Deprivation in Kittens
• 2. Infant Precursors of Later Visual Disorders: Correlation or Causality?
• 3. Anatomical Constraints on Oculomotor Development: Implications for Infant Perception
• 4. Sensory Selectivity, Attentional Control, and Cross-Channel Integration in Early Visual Development
• 5. Visual Recalibration and the Development of Contrast and Optical Flow Perception
• 6. Where Perceiving Ends and Thinking Begins: The Apprehension of Objects in Infancy
• 7. Speech as an Intermodal Object of Perception
• 8. Theories of Perception and Research in Perceptual Development
• 9. Levels of Description and Constraints on Perceptual Development
• Author Index
• Subject Index