Experience-dependent maturation of the spatial and temporal characteristics of the cell receptive fields in the kitten visual cortex.

The development of contrast sensitivity to spatial and temporal frequencies was studied in the visual cortex of 6-week-old kittens reared from birth in three conditions: normal, dark-reared (DR) and dark-reared after 6 h of visual experience. Receptive fields of cells recorded in area 17 were quantitatively analysed using drifting sine-wave gratings. Compared to the low values obtained in the DR kittens, we observed after 6 h of visual experience: (1) an adult-like detection of higher spatial frequencies, (2) an increase of contrast sensitivity at low temporal frequencies; (3) a shift of the cell optimum towards 3 Hz, all values close to the normal ones. Unlike the spatial frequency selectivity, contrast sensitivity and detection of higher temporal frequencies continue to develop with age and visual experience.

Long-term effects of dark rearing on a visually guided reaching movement in cats.

The existence of long-term effects of dark-rearing on visuo-motor coordination is still controversial. In this study 2 dark-reared (DR) cats were trained, after 5-6 years of recovery, to perform a reaching movement towards a stationary or a moving target. The accuracy, and the reaction and movement times were evaluated. The scores obtained by the DR cats were compared to those of normal subjects after a similar period of training. The results showed that while the accuracy of DR cats was not impaired, the performance of their reaching movements was slower than normal and its triggering was delayed. These data are discussed with regards to electrophysiological and behavioural data obtained on analogous DR cats after long-term recovery.

Temporal correlations in modulated evoked responses in the visual cortical cells of the cat.

We analysed evoked responses recorded from 97 cells in the visual cortex of 4 adult cats and 8 kittens, stimulated by a drifting sinusoidal grating. A Fourier analysis of the responses allowed us to select 30 cells showing a clear modulating response (relative modulation index greater than 1). The 162 records from these selected cells were scanned to detect precise temporal correlations in the form of replicating triplets and associated "ghost" doublets. Temporal correlations of this nature were observed in these cells. They are about 10 times more abundant in adult cats than in kittens, and mostly observed in infragranular cortical layer cells. The possible role of these precise temporal patterns in information processing in the brain is examined, as well as the relation between this type of temporal correlation with coherent oscillations and principal components waveforms.

Area centralis position relative to the optic disc projection in kittens as a function of age.

Changes during development of the optic disc projection relative to the area centralis position in the visual field were studied in the kitten. The determinations were based both on direct measurement and physiological location of these retinal landmark projections. The results showed that the relative distance between these retinal landmarks in visual space became shorter with age, indicating that the visual field coordinates change extensively with age. Since the area centralis cannot be seen in most young kittens, the mean distances we have determined for the landmarks in the visual field may provide a useful means of estimating the position of area centralis from the projected position of the optic disc. Our results also confirm the nonuniform growth of the retina suggested already from anatomical observations. Taking into account both eye growth and the changes in the visual field coordinates allowed some reinterpretation of changes in physiological properties of the visual cells known to occur during development, such as decreased size of the visual receptive fields, increased spatial resolution and increased responsiveness to high velocity visual stimuli.

Visual field in dark-reared cats after an extended period of recovery.

The visual field of dark-reared cats was behaviourally measured after several years of recovery in a normal environment. A reduction of the visual field was observed and affected the contralateral field as well as the ipsilateral field when tested in monocular viewing. The longer the deprivation period, the more reduced was the visual field. Our results suggest that binocular deprivation might have stabilized the visual system in an immature state.

Comparative development of cell properties in cortical area 18 of normal and dark-reared kittens.

The development of visual cell properties was studied in cortical Area 18 (A18) of normal (NRs) and dark-reared kittens (DRs), from 2 weeks of age to adulthood. In addition to the orientation selective (S) and non-selective (NS) cells, we describe a new type of non-selective cell with a peripheral zone (NSp), which could be either an intermediate form between NS and S cells and included in a sequential model or an immature form of the S cells whose responses are affected by peripheral stimulations. Using accurate coordinates for the area centralis position relative to the optic disc projection as a function of age, we show that: a) the extent of the visual field increases with age in DRs and NRs; b) the retinotopic organization is always present; c) receptive fields, large in the NS cells, reduce to the size of mature S cells as soon as the cells acquire orientation selectivity. This process can occur after only 6 h of visual experience; d) velocity preference shifts toward high velocities, though more so in NRs than in DRs. An interpretation of the development of these properties is proposed, taking into account eye growth, the growth of dendritic fields and the formation of new connections. A comparison with previous results obtained in Area 17 (A17) shows a similar time course of the specification (NRs) and of the despecification (DRs) processes, although the development of A18 is postponed by about 2 weeks. Moreover, the "adult-like" binocular distribution of ocular dominance depends upon visual experience in A18, while it does not in A17.

Development of the kitten visual cortex depends on the relationship between the plane of eye movements and visual inputs.

1. Previous experiments have demonstrated that eye movements, acting through the extraocular muscle (EOM) proprioceptive afferents, are necessary for the development of orientation selectivity in the cells of the kitten visual cortex. New experiments were carried out to study the effect of the plane of eye movements on the preferred orientation acquired by the visual cortical cells. 2. Dark-reared (DR) kittens were operated on at 5-6 weeks of age. In the first series of experiments, 4 out of the 6 EOMs were removed bilaterally in such a way that both eyes could only move in a single plane, either vertical or horizontal. In the second series of experiments, the same operation was performed on one eye which was also sutured shut and, on the other side, the EOM were deafferented by intracranial section of the ophthalmic branch of Vth nerve and the eye left open. 3. 1-4 days after surgery the kittens were given 6 h of visual experience and 12 h later were prepared for visual cell recording in Area 17. 4. In kittens of the first series: orientation selectivity developed in the majority (60-65%) of visual cells, most of which encoded horizontal orientations when the eyes had moved in the vertical plane and vertical orientations when the eyes had moved in the horizontal plane. These results show that the plane of eye movements during early visual experience influences the distribution of preferred orientations with an orthogonal relation. Ocular dominance histograms were "strabismic like". 5. In kittens of the second series: orientation selectivity developed in 40-50% of cells, about half of which were tuned for the orientation orthogonal to the direction of movement of the occluded eye, as in experiment I. The seeing, deafferented eye, presumably would have sent normal visual inputs centrally, corresponding to displacements on the retina in every direction since the ocular motility of that eye had not been disturbed. However, proprioceptive information about its movements was suppressed. As only some of the EOMs of the occluded eye were still present and connected, the conclusion is that the observed influence of the plane of eye movements acts through the proprioceptive afferents.(ABSTRACT TRUNCATED AT 400 WORDS)

[Response of neurons of the visual cortex (area 18) to extraocular proprioceptive stimulation: development in normal or dark-reared cats and interaction with visual activity]. / Réponses des neurones du cortex visuel (Aire 18) aux stimulations proprioceptives extraoculaires: évolution chez le chat normal ou élevé à l'obscurité et interactions avec l'activité visuelle.

Single unit responses to stimulation of the extraocular muscle receptors or of their afferent fibers were recorded from the visual cortical area 18 in normally or dark-reared cats. These responses were improved by a random visual stimulation delivered during the test. These proprioceptive responses, elicited with or without random visual activation, changed with age and as a function of the postnatal rearing conditions. In the normally-reared group, neurons which were activated by stimulation of the afferents from the Obliquus inferior displayed a preferred orientation for visual stimulus oriented at right angle to action plane of this particular muscle.

Role of eye movements in developmental processes of orientation selectivity in the kitten visual cortex.

Six-week-old dark-reared kittens were exposed for 6 hr to a normal lighted environment in which they were free to move, but with eyes immobilized. Receptive field properties (orientation selectivity and ocular dominance) of the visual cortical cells (Area 17) were studied. No restoration of orientation selectivity could be observed when only the eyes were immobilized either by oculomotor nerve sections or by extraocular muscles removal, in contrast to what had been observed in intact free moving animals. From these results one can conclude that eye movements must be associated with vision to allow developmental processes of orientation selectivity in the primary cortex. These new results are compared to those obtained previously in paralyzed or restrained animals and those obtained in animals with interruption of orbital afferents.

Noradrenaline and functional plasticity in kitten visual cortex: a re-examination.

A quantitative re-examination was made of the influence of noradrenergic depletion on the epigenesis of kitten visual cortex. Two methods were used to deplete noradrenaline at the cortical level: stereotaxically controlled injection of 6-hydroxydopamine (6-OHDA) in the coeruleus complex, from which the noradrenergic input to visual cortex arises; intraventricular injection of 6-OHDA. The latter chemical lesion also depleted dopamine levels in the brain. Lesion of the noradrenergic or catecholaminergic systems was performed neonatally or at an age of 3-4 weeks in kittens submitted to five different rearing procedures: normal rearing, dark rearing, monocular rearing, monocular exposure following dark rearing and monocular deprivation following normal rearing. Forty-two kittens between 3 and 12 weeks of age were used for this biochemical and electrophysiological study. Noradrenaline and dopamine levels were measured by a radioenzymatic method in the primary visual cortex of twenty-six kittens. A total of 1263 cells were recorded in area 17 of twenty-six kittens. Combined biochemical and electrophysiological data were obtained in ten 6-OHDA-lesioned kittens. Whatever the mode of chemical lesion used, cortical noradrenergic depletion failed to block either maturation or vision-dependent processes which are known to affect orientation selectivity and/or ocular dominance during the critical period. However, in some cases, the amplitude of the epigenetic functional modifications was slightly reduced in 6-OHDA-treated kittens. The cortical effects of monocular deprivation starting from the age of 5 weeks were studied quantitatively both in lesioned and intact kittens. Disappearance of noradrenaline in area 17 did not prevent the loss of binocularity in cortical cells. However, even when monocular occlusion had been maintained for 2 or 3 weeks in 6-OHDA-treated kittens, ocular dominance shifts were limited to a stage equivalent to that observed in the intact kitten after 5-8 days of monocular occlusion. The amplitude of this partial protective effect was found to be unrelated either to the delay following the chemical lesion, or to the level of noradrenaline remaining in lesioned kitten cortex. Although a putative gating role of noradrenaline cannot be excluded in the development of the intact animal, this report shows that its presence is not required for functional plasticity to occur in kitten area 17.

[Postnatal development of functional properties of the visual cortical cells of area 18 in kittens raised with or without visual experience]. / Développement post-natal des propriétés fonctionnelles des cellules visuelles corticales de l'aire 18 chez le chaton élevé avec ou sans expérience visuelle.

866 units were recorded extracellularly in area 18 of anaesthetized and paralysed kittens from 13 to 66 days of age. The development of their receptive field properties was studied in normally (EN) and dark-reared (EO) kittens. In addition to orientation selective (S) and non-selective (NS) cells, we found a number of non-selective units whose receptive field was surrounded by a peripheral zone (NSp) where stationary stimuli were effective. In EN kittens, the orientation selectivity developed with age and concomitantly, NS and NSp cells disappeared. Ocular dominance distribution was also gradually modified from a contralateral monocular dominance at 13 days of age to an adult-like binocularity at 58 days. In EO kittens, the early orientation selectivity began to decrease at the 5th week. From then on, the process of despecification started and progressed until nearly all cells were NS. Absence of visual experience also delayed the development of mature binocularity. In 6 week old EO kittens, a 6 hrs. visual exposure induced a fast but uncomplete specification with decrease of both NS and NSp cells and a slight modification of the ocular dominance distribution. The comparison of these results with those obtained in area 17 shows that functional properties vary more slowly in area 18 than in area 17.

[Noradrenaline and plasticity of the visual cortex of the kitten: a reexamination]. / Noradrénaline et plasticité du cortex visuel du Chaton: un réexamen.

We have undertaken a study of the role of the noradrenergic system in the functional modifications, observed in the primary visual cortex of the Kitten, following monocular deprivation. The lids of one eye were sutured in 5 week old Kittens for a period of 1 or 2 weeks. Noradrenergic depletion was obtained by 6-OHDA injection, either intraventricular or localized in the coeruleus complex. Our results indicate that disappearance of noradrenaline in area 17 does not prevent the loss of binocularity of cortical cells, but appears to limit ocular dominance shifts at a stage equivalent to that observed in the intact Kitten after 6 days of monocular deprivation.

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.

Recovery of orientation selectivity in kitten primary visual cortex is slowed down by bilateral section of ophthalmic trigeminal afferents.

The recovery of orientation selectivity in the primary visual cortex has been studied in 6-week-old dark-reared (DR) kittens after visual exposure of various durations following bilateral section of either the ophthalmic (V1) or the maxillary (V2) branches of the Vth nerve. After 6 h of vision, visual cortical neurones become orientation selective in V2-operated kittens as well as in intact animals, while they remain non-specific in V1-operated kittens. However, in this latter case, if the duration of visual exposure is extended to 4 weeks, a slow and incomplete recovery of orientation selectivity takes place.

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

The 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.

Development of visual cortical orientation specificity after dark-rearing: role of extraocular proprioception.

Six-week-old dark reared kittens exposed to light for 6 h: (1) with head and body tightly cast into plaster; or (2) free to move around in the animal room. A few days before the visual experience, the ophthalmic branch of the 5th nerve was severed bilaterally in experimental kittens, in order to suppress most of the proprioceptive afferents from extraocular muscles. Electrophysiological analysis of the properties of the receptive fields of visual cortical cells shows that only 6% (group 1) and 11% (group 2) of the cells were selective to orientation as opposed to 67% (group 1) or 32% (group 2) observed in the non-operated kittens.