Michel Imbert

Receptive field characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience

SummaryThe functional organization of visual cortical cells was studied in two groups of five week old kittens: one group normally reared, the other reared in total darkness from the third day after birth. The following results were obtained:1.The cells of the normally reared kittens were similar to adult cells except for some aspects of immaturity. In contrast, the cells of the dark-reared kittens were totally non-specific. Their receptive field showed neither orientational nor directional properties.2.The distribution of cells according to the ocular dominance was not different in either group and was similar to that previously described for ‘adult’ cells.3.A few hours of visual experience was sufficient to provide specific receptive field properties to the cortical cells of a dark-reared kitten.4.Conditioning exposure with an oriented grating induced changes in orientational sensitivity in normally reared kittens but not in dark-reared kittens.

Plasticity in the kitten's visual cortex: effects of the suppression of visual experience upon the orientational properties of visual cortical cells.

The orientation selectivity of visual cortical cells was tested in two groups of kittens. In one group the animals were reared normally for the first 4-6 weeks of life then kept in darkness. Those in the other group were dark-reared for the first 6 weeks then exposed to light for 6 h and returned to the dark. The properties of the receptive fields of visual cortical cells were examined in these kittens after periods of dark-rearing ranging from 3 days to 12 weeks. In both groups, the proportion of orientation selective cells was found to decrease with time spent in the dark. The critical period for orientation appeared to end at 10-12 weeks of age. Two populations of visual cells were distinguished functionally by their different behaviour during prolonged dark-rearing. Most of the cells which retained their orientation specificity longest during dark-rearing were tuned to horizontal or vertical orientations and more of them were monocular than in normal kittens. These functional characteristics resemble those exhibited by neurons of very young kittens. Changes in specificity observed during loss of selectivity are compared to those observed during early development. We suggest that the extent to which the orientation selectivity of a cell is plastic depends very largely upon the time, during the course of development, at which its selectivity was acquired.

Lesion of the PGO pathways in the kitten. II. Impairment of physiological and morphological maturation of the lateral geniculate nucleus

Suppression of the geniculate ponto-geniculo-occipital (PGO) waves by bilateral lesions of PGO pathways at the mesencephalic level in 15-day-old kittens has been shown to induce a significant reduction of the mean discharge frequency recorded in the lateral geniculate nucleus (LGN) during paradoxical sleep. The present paper reports that one month after the bilateral lesion (i.e., 6-7 weeks of age) important deficits in the maturation of the LGN were observed: (1) electrophysiologically, the latencies of the LGN cellular responses to stimulation of the optic chiasm were significantly longer than those of age-paired controls or of unilaterally lesioned animals, and the proportion of visual cells characterized as type X by stimulation of the visual field was smaller; and (2) morphologically, the volume of the LGN and the size of its neuronal somata were smaller than those in control. These data suggest that bilateral suppression of extraretinal PGO afferents to the LGN in the kitten induces a significant delay in the development of this nucleus.

Effect of neonatal unilateral enucleation on the development of orientation selectivity in the primary visual cortex of normally and dark-reared kittens

SummaryThe developmental properties of 573 neurones have been investigated in the primary visual cortex of eight binocularly intact and twelve unilaterally enucleated kittens. It is shown that removal of one eye at birth alters the development of orientation selectivity observed in the presence or absence of visual experience. In 6-week-old deprived kittens, there remain significantly more orientation selective cells in enucleated than in binocularly deprived kittens. These deprivation-resistant cells respond preferentially to horizontal or vertical orientations and are recorded mainly in the cortex contralateral to the remaining eye. In six-week-old kittens with visual experience, the process of tuning maturation appears to be unaffected by unilateral enucleation at birth. However, a larger over-representation of horizontal and vertical orientation preferences is observed in uniocular kittens than in binocularly intact kittens, suggesting that the development of oblique orientation preference depends upon the presence of binocular afferents in the visual pathway.

Maturation of Visual Cortex with and without Visual Experience

The evolution of the response properties of visual cortical cells was studied in two groups of kittens between 1 and 7 weeks of age—one group normally reared, the other reared in complete darkness. Four classes of striate neurones were defined: (a) non-activatable cells, (b) non-specific cells, (c) immature cells, (d) specific cells that are as selective for orientation as the simple or complex cells of the adult cat. The results confirm that as soon as neurones become visually activated, about 25% of the recorded visual units are definitely specific in terms of orientation selectivity. These neurones are present in earliest stages, even in the absence of any visual experience. However, active visual experience (visuomotor interaction) is necessary to maintain and develop these specific cells after the third week of postnatal life. Polar diagrams of the orientation encoded by specific cells show that for kittens under 3 weeks of age and whatever the rearing condition, there are more specific cells coding horizontal or vertical orientation than those coding oblique orientations. These horizontally and vertically oriented cells are preferentially driven by the contralateral eye. Thus, the ocular dominance distribution and the orientation selectivity appear as two linked parameters characterizing visual specificity in very young kittens independently of any visual experience. An hypothesis of “differential modifiability” is proposed: contralateral monocular “horizontal and vertical detectors” are supposed to be stable. They would remain so until they become binocular. Binocular cells, for which competition between two inputs occurs, are the labile units which can be despecified or be specified under the control of visual experience.

Temporal limits of the susceptibility of depth perception to proprioceptive deafferentations of extraocular muscles

In a previous study, extraocular muscle proprioception (E.O.M.P.) was shown to play an important role in the postnatal development of depth perception: following unilateral or bilateral sections of the ophthalmic branch of the trigeminal nerve (V1th nerve) performed at 6-8 weeks of age, the binocular thresholds were 2 to 3 times higher than in control animals. Since the V1-sections produced no deficits when performed in adults, the temporal limits of a period of susceptibility remained to be determined. In order to assess the lower and upper limits of the period during which these perceptual deficits could be induced, unilateral or bilateral V1-sections were performed in kittens at different ages. Depth perception thresholds were measured by using the jumping stand technique. Sections of the V1 nerve only produced significant impairments of the binocular depth thresholds when performed after 3 weeks of age. They could be observed when unilateral sections were performed at up to 13 weeks of age and with bilateral sections at up to 10 weeks of age. These functional impairments appeared to remain permanently through adult life.

Visually triggered oculomotor discharges with and without eye movements

Abstract A visual stimulus, a complex contrasted form, applied in the periphery of the visual field of an unanesthetized cat is used in order (1) to determine whether this visual stimulus is capable of triggering the ocular movements of fixation and/or tracking, (2) to evaluate the efferent discharge of the oculomotor nerves associated with these movements, (3) to compare the efferent discharge in the non-paralyzed animal with that in the curarized animal. A comparison of the nerve discharges before and after curarization shows that the fact that the movement is not performed has an effect on the pattern of discharge.