Recovery from monocular deprivation in the monkey. I. Reversal of physiological effects in the visual cortex

This is a study of the effects of monocular deprivation, reverse suturing (opening the deprived eye with closure of the other) and reopening of the deprived eye alone (without closing the other) on the physiological organization of the primary visual cortex in monkeys (Erythrocebus patas). All animals were initially monocularly deprived by suture of the lids of the right eye from soon after birth until about 4 weeks of age (24-29 days). In a monocularly deprived animal, recordings were taken from area 17 at 24 days. Already most neurons recorded outside layer IVc, were strongly or completely dominated by functional input from the left eye. The Non-oriented cells of layer IVc, where the bulk of the afferent input terminates, were also mainly dominated by the left eye. Although segregation of input from the two eyes was not complete, large areas of layer IVc were already monocularly dominated by the left eye. Four animals were reverse-sutured at about 4 weeks and recorded 3, 6, 15 and 126 days later. In each animal the pattern of ocular dominance was fairly similar within and outside layer IVc. Even with only 3 days of forced usage of the initially deprived right eye, about half of all cells recorded had become dominated by it, and the process of "recapture' of cortical cells by the initially deprived eye was apparently complete within 15 days. In layer IVc, the recovery took the form of an expansion of zones dominated by the deprived eye, as if the originally shrunken stripes of afferent termination had become enlarged. Binocularly driven neurons were rare at all stages, in all layers, but when present and orientation-selective, they had similar preferred orientations in the two eyes. Likewise the "columnar' sequences of preferred orientation continued without obvious disruption on shifting from regions dominated by one eye to those dominated by the other. Simply reopening the deprived eye at about 4 weeks, for 15 to 96 days caused no detectable change in the overall ocular dominance of cortical cells and, on average, no expansion of right-eye dominance columns in layer IVc. Therefore the recovery seen after reverse suturing depends not just on the restoration of normal activity to axons carrying information from the right eye, but on the establishment of a competitive advantage, through the right eye being made more active than the left.     

Recovery from monocular deprivation in the monkey. II. Reversal of morphological effects in the lateral geniculate nucleus

The cross-sectional area was measured of neurons in the lateral geniculate nucleus (l.g.n.) of monkeys (Erythrocebus patas) subjected to monocular deprivation by unilateral eyelid suture, and of others in which the closed lids had been subsequently opened (either alone, "reopening', or together with closure of the previously open eye, "reverse suture'). Monocular deprivation for the first month of the monkey's life retards l.g.n. cell growth such that neurons in the laminae innervated by the closed eye are about 15% smaller in cross-sectional area than those in normally innervated laminae. This failure of normal growth can be countered by reverse suture for even short periods of time, the size difference between laminae being abolished within 6 days after reverse suture performed at the age of 1 month. Simply reopening the closed eye has little or no effect on l.g.n. neuronal recovery. These morphological results in the l.g.n. correlate closely with studies on the width of ocular dominance "stripes' in layer IVc of the visual cortex of the same animals: the stripes, narrower than normal after monocular deprivation, "expand' with a time course similar to that of l.g.n. cell recovery, as judged by single unit recording and by autoradiography in the cortex after transneuronal transport of labelled tracers injected in an eye.     

How monocular deprivation shifts ocular dominance in visual cortex of young mice

We used a chronic recording method to document the kinetics of ocular dominance (OD) plasticity induced by temporary lid closure in young mice. We find that monocular deprivation (MD) induces two separate modifications: (1) rapid, deprivation-induced response depression and (2) delayed, deprivation-enabled, experience-dependent response potentiation. To gain insight into how altering retinal activity triggers these cortical responses, we compared the effects of MD by lid closure with monocular inactivation (MI) by intravitreal injection of tetrodotoxin. We find that MI fails to induce deprived-eye response depression but promotes potentiation of responses driven by the normal eye. These effects of MI in juvenile mice closely resemble the effects of MD in adult mice. Understanding how MI and MD differentially affect activity in the visual system of young mice may provide key insight into how the critical period ends.     

Recognition of visual stimuli from multiple neuronal activity in monkey visual cortex

Response patterns recorded with 30 microelectrodes from area 17 of anaesthetized monkeys are analysed. A proportion of the patterns are used to define prototype response patterns. These in turn are used to recognize the stimulus from further non-averaged response patterns. In comparison, recognition by a feedforward neural network is much slower, and slightly inferior. The excitation time structure, with a resolution of about 20 ms, is found to contribute strongly to the recognition. There is some inter-ocular recognition for oriented moving bars, and for on and off phases of switched lights, but none for colours. Generalizations over some stimulus parameters (i.e. cases of confusion) are examined: If small jerking shapes are incorrectly recognized, in general the jerk direction often is the correct one. The onset of a response can most easily be found by determining the dissimilarity relative to spontaneous activity in a sliding window.     

The effect of visual deprivation upon the basal dendrites of Meynert cells in the striate cortex of the monkey

The basal dendrites of Meynert cells in the striate cortex have been studied with the Golgi method in the brains of monkeys that had been reared for varying periods with the eyelids closed over one eye. The lengths and arrangement of the dendrites were compared with those in normal brains. In the visually deprived brain almost half of the cells had basal dendrites that were apparently normal with the dendritic fields in the form of an ellipse and the long axes parallel to the direction of the ocular dominance bands. The other cells had dendritic fields that have rarely been seen in normal material and two distinct types could be recognized. The 'lop-sided' cell had an ellipsoidal dendritic field with the major axis parallel to the ocular dominance bands, but the extents of the dendrites along the minor axis were very asymmetric; the ratio of the means of the long and short arms of the minor axis of the 'lop-sided' cell is 2.3:1 compared with 1.1:1 in normal brains. The 'perpendicular' type of cell also had an ellipsoidal dendritic field but the relation of the major and minor axes to the direction of the ocular dominance bands was the reverse of the normal cell, with the long axis of the ellipse being aligned perpendicular to the bands. 'Lop-sided' cells formed approximately 18% of the total of Meynert cells studied and the 'perpendicular' 32%. The proportion of the cells with abnormal basal dendritic fields, and particularly the 'perpendicular', increased with longer durations of eyelid closure. It is suggested that the alterations in the dendritic fields of the 'lop-sided' and 'perpendicular' cells may be correlated with the changes in width of the ocular dominance bands that are known to occur after monocular eyelid suture.     

Acetylcholinesterase activity in visual cortex structures during early visual deprivation

By means of quantitative histochemical methods it has been shown that an early photic deprivation (animals kept in a dark chamber for two months after their birth) leads to a decrease in the activity level of acetylcholinesterase (AChE) in the visual area of the cerebral cortex. With the recovery of the visual function (animals kept in normal photic conditions for two weeks) the AChE activity becomes markedly normalized. The obtained data allow to suggest that the decrease in AChE activity due to deprivation is functionally determined.     

Some Golgi data on visual cortex of the rhesus monkey.

The rhesus monkey's visual cortex was studied on Golgi material. The terminal arborization of the geniculate fibres and non-specific vertical fibres have been analysed. The interneurons (intrinsic neurons) of the area described in detail and classified on the basis of their axonal and dendrite arborizations. The stellate neurons in layer IV are discussed.     

Effects of attention on the reliability of individual neurons in monkey visual cortex.

To determine the physiological mechanisms underlying the enhancement of performance by attention, we examined how attention affects the ability of isolated neurons to discriminate orientation by investigating the reliability of responses with and without attention. Recording from 262 neurons in cortical area V4 while two rhesus macaques did a delayed match-to-sample task with oriented stimuli, we found that attention did not produce detectable changes in the variability of neuronal responses but did improve the orientation discriminability of the neurons. We also found that attention did not change the relationship between burst rate and response rate. Our results are consistent with the idea that attention selects groups of neurons for a multiplicative enhancement in response strength.     

Effect of visual deprivation on evoked potentials in the visual cortex and superior colliculus in rabbits

Evoked potentials arising in the visual cortex and superior colliculus to stimulation of the collateral eye by single, paired, and repetitive flashes were recorded in rabbits reared in darkness or in normal illumination. The absence of significant change in the latent period and amplitudes of the first two components of the collicular responses and of the recovery cycle and response to repetitive stimulation in the light-deprived animals suggest that photic stimulation does not affect the normal functional development of the rabbit retinotectal system. However, functional deafferentation in the early postnatal period gives rise to serious disturbances of visual cortical function, as reflected in a marked decrease in amplitude of the primary response, lengthening of the recovery cycle, and narrowing of the range of rhythm-binding frequencies of flashes. These disturbances were reversible. The period of maximal sensitivity of the rabbit retinocortical system to visual deprivation begins at the end of the first month of postnatal life. The possible mechanisms lying at the basis of these functional disturbances in light-deprived animals are discussed.     

Biochemical differences in the reactions of visual cortex neurons to deprivation]

Early visual deprivation was interferometrically shown to entail changes in the concentration and contents of the protein substance with simultaneous changes of the neurons size. The changes are statistically significant in the lamina V and not in the laminasIII and IV. The changes in each lamina are associated with definite group of the neurons the development of which is, probably, determined by visual stimuli.     

Fucntional specialization and binocular interaction in the visual areas of rhesus monkey prestriate cortex.

If is is believed that neural mechanisms mediating stereoscopic vision may be localized in specific areas of the visual cortex, then it becomes necessary to be able to define these areas adequately. This is no easy matter in the rhesus monkey, an animal close to man, where the cytoarchitecturally uniform prestriate cortex is folded into deep sulci with secondary gyri. One way around this awkward problem is to use the callosal connections of the prestriate cortex as the anatomical landmarks. Callosal connections are restricted to regions at which the vertical meridian is represented. Since the visual fields, including the vertical meridian, are separately represented in each area, each has its own callosal connections. These are of great help in defining some of the boundaries of these areas, since the boundaries often coincide with the representation of the vertical meridian. With the visual areas thus defined anatomically, it becomes relatively easy to assign recordings to particular areas. Studies of binocular interactions in these areas reveal that most cells in all prestriate areas are binocularly driven. Hence, theoretically, all of the prestriate areas are candidates for stereoscopic mechanisms. The degree of binocular interaction varies from cell to cell. At the two extremes are cells which either respond to monocular stimulation only and are inhibited by binocular stimulation or ones which respond to binocular stimulation only. Changing, as opposed to fixed, disparity is signalled by two types of cells. In one category are cells activated in opposite directions for the two eyes. Such cells are always binocularly driven. In the other category are cells, some of which are monocularly activated, that are capable of responding to changing image size. In the monkey, both these categories of cells have so far been found in the motion area of the superior temporal sulcus only.