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Journal Article•DOI•

The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat

01 Aug 1970-The Journal of Comparative Neurology (J Comp Neurol)-Vol. 139, Iss: 4, pp 413-421
TL;DR: The observations are consistent with the view that during normal development geniculate cell axons from adjacent laminae compete with each other for synaptic surfaces upon binocular cortical neurons: that unilateral lid suture upsets the balance of this competition and that the reduced perikaryal growth in the lateral geniculated nucleus is secondary to the unbalanced axonal development.
Abstract: One eyelid has been sutured in each of three seven-day old kittens. Three months later the brains were fixed and stained by the Nissl method. In the contralateral lateral geniculate nucleus the cells of the deprived lamina A were smaller, more closely packed and paler staining than those in the normally innervated, ipsilateral lamina A. However, these changes were seen in the medial parts of the contralateral lamina A only. The lateral parts, which extend beyond the border of lamina A1 and which project to the monocular parts of the visual cortex showed no change. These results show that some geniculate cells are not affected by deprivation. The observations are consistent with the view that during normal development geniculate cell axons from adjacent laminae compete with each other for synaptic surfaces upon binocular cortical neurons: that unilateral lid suture upsets the balance of this competition and that the reduced perikaryal growth in the lateral geniculate nucleus is secondary to the unbalanced axonal development, which occurs in the binocular portions of the geniculocortical projection but which cannot occur in the monocular portions, where there is no competition.
Citations
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Journal Article•DOI•
TL;DR: In most respects the above description fits the newborn monkey just as well as the adult, suggesting that area 17 is largely genetically programmed.
Abstract: Of the many possible functions of the macaque monkey primary visual cortex (striate cortex, area 17) two are now fairly well understood. First, the incoming information from the lateral geniculate bodies is rearranged so that most cells in the striate cortex respond to specifically oriented line segments, and, second, information originating from the two eyes converges upon single cells. The rearrangement and convergence do not take place immediately, however: in layer IVc, where the bulk of the afferents terminate, virtually all cells have fields with circular symmetry and are strictly monocular, driven from the left eye or from the right, but not both; at subsequent stages, in layers above and below IVc, most cells show orientation specificity, and about half are binocular. In a binocular cell the receptive fields in the two eyes are on corresponding regions in the two retinas and are identical in structure, but one eye is usually more effective than the other in influencing the cell; all shades of ocular dominance are seen. These two functions are strongly reflected in the architecture of the cortex, in that cells with common physiological properties are grouped together in vertically organized systems of columns. In an ocular dominance column all cells respond preferentially to the same eye. By four independent anatomical methods it has been shown that these columns have the from of vertically disposed alternating left-eye and right-eye slabs, which in horizontal section form alternating stripes about 400 $\mu $m thick, with occasional bifurcations and blind endings. Cells of like orientation specificity are known from physiological recordings to be similarly grouped in much narrower vertical sheeet-like aggregations, stacked in orderly sequences so that on traversing the cortex tangentially one normally encounters a succession of small shifts in orientation, clockwise or counterclockwise; a 1 mm traverse is usually accompanied by one or several full rotations through 180 degrees, broken at times by reversals in direction of rotation and occasionally by large abrupt shifts. A full complement of columns, of either type, left-plus-right eye or a complete 180 degrees sequence, is termed a hypercolumn. Columns (and hence hypercolumns) have roughly the same width throughout the binocular part of the cortex. The two independent systems of hypercolumns are engrafted upon the well known topographic representation of the visual field. The receptive fields mapped in a vertical penetration through cortex show a scatter in position roughly equal to the average size of the fields themselves, and the area thus covered, the aggregate receptive field, increases with distance from the fovea. A parallel increase is seen in reciprocal magnification (the number of degrees of visual field corresponding to 1 mm of cortex). Over most or all of the striate cortex a movement of 1-2 mm, traversing several hypercolumns, is accompanied by a movement through the visual field about equal in size to the local aggregate receptive field. Thus any 1-2 mm block of cortex contains roughly the machinery needed to subserve an aggregate receptive field. In the cortex the fall-off in detail with which the visual field is analysed, as one moves out from the foveal area, is accompanied not by a reduction in thickness of layers, as is found in the retina, but by a reduction in the area of cortex (and hence the number of columnar units) devoted to a given amount of visual field: unlike the retina, the striate cortex is virtually uniform morphologically but varies in magnification. In most respects the above description fits the newborn monkey just as well as the adult, suggesting that area 17 is largely genetically programmed. The ocular dominance columns, however, are not fully developed at birth, since the geniculate terminals belonging to one eye occupy layer IVc throughout its length, segregating out into separate columns only after about the first 6 weeks, whether or not the animal has visual experience. If one eye is sutured closed during this early period the columns belonging to that eye become shrunken and their companions correspondingly expanded. This would seem to be at least in part the result of interference with normal maturation, though sprouting and retraction of axon terminals are not excluded.

2,314 citations

Journal Article•DOI•
TL;DR: The results indicated that the deprivation caused by monocular suture produced a decrease in the cytochrome oxidase staining of the binocular segment of the deprived geniculate laminae of kittens, leading to a significant decreases in the level of oxidative enzyme activity one to several synapses away.

1,862 citations

Journal Article•DOI•
TL;DR: Preliminary experiments suggest that the layer IVC columns in juvenile macaque monkeys are not fully developed until some weeks after birth, which explains the critical period for deprivation effects in the layerIV columns.
Abstract: Ocular dominance columns were examined by a variety of techniques in juvenile macaque monkeys in which one eye had been removed or sutured closed soon after birth. In two monkeys the removal was done at 2 weeks and the cortex studied at 1\frac{1}{2} years. Physiological recordings showed continuous responses as an electrode advanced along layer IVC in a direction parallel to the surface. Examination of the cortex with the Fink-Heimer modification of the Nauta method after lesions confined to single lateral-geniculate layers showed a marked increase, in layer IVC, in the widths of columns belonging to the surviving eye, and a corresponding shrinkage of those belonging to the removed eye. Monocular lid closures were made in one monkey at 2 weeks of age, for a period of 18 months, in another at 3 weeks for 7 months, and in a third at 2 days for 7 weeks. Recordings from the lateral geniculate body showed brisk activity from the deprived layers and the usual abrupt eye transitions at the boundaries between layers. Cell shrinkage in the deprived layers was moderate - far less severe than that following eye removal, more marked ipsilaterally than contralaterally, and more marked the earlier the onset of the deprivation. In autoradiographs following eye injection with a mixture of tritiated proline and tritiated fucose the labelling of terminals was confined to geniculate layers corresponding to the injected eye. Animals in which the open eye was injected showed no hint of invasion of terminals into the deprived layers. Similarly in the tectum there was no indication of any change in the distribution of terminals from the two eyes. The autoradiographs of the lateral geniculates provide evidence for several previously undescribed zones of optic nerve terminals, in addition to the six classical subdivisions. In the cortex four independent methods, physiological recording, transneuronal autoradiography, Nauta degeneration, and a reduced-silver stain for normal fibres, all agreed in showing a marked shrinkage of deprived-eye columns and expansion of those of the normal eye, with preservation of the normal repeat distance (left-eye column plus right-eye column). There was a suggestion that changes in the columns were more severe when closure was done at 2 weeks as opposed to 3, and more severe on the side ipsilateral to the closure. The temporal crescent representation in layer IVC of the hemisphere opposite the closure showed no obvious adverse effects. Cell size and packing density in the shrunken IVth layer columns seemed normal. In one normal monkey in which an eye was injected the day after birth, autoradiographs of the cortex at 1 week indicated only a very mild degree of segregation of input from the two eyes; this had the form of parallel bands. Tangential recordings in layer IVC at 8 days likewise showed considerable overlap of inputs, though some segregation was clearly present; at 30 days the segregation was much more advanced. These preliminary experiments thus suggest that the layer IVC columns are not fully developed until some weeks after birth. Two alternate possibilities are considered to account for the changes in the ocular dominance columns in layer IVC following deprivation. If one ignores the above evidence in the newborn and assumes that the columns are fully formed at birth, then after eye closure the afferents from the normal eye must extend their territory, invading the deprived-eye columns perhaps by a process of sprouting of terminals. On the other hand, if at birth the fibres from each eye indeed occupy all of lay IVC, retracting to form the columns only during the first 6 weeks or so, perhaps by a process of competition, then closure of one eye may result in a competitive disadvantage of the terminals from that eye, so that they retract more than they would normally. This second possibility has the advantage that it explains the critical period for deprivation effects in the layer IV columns, this being the time after birth during which retraction is completed. It would also explain the greater severity of the changes in the earlier closures, and would provide an interpretation of both cortical and geniculate effects in terms of of competition of terminals in layer IVC for territory on postsynaptic cells.

1,567 citations

01 Jan 1977
TL;DR: By four independent anatomical methods it has been shown that these columns have an ocular dominance column all cells respond preferentially to the same eye, in that cells with common physiological properties are grouped together in vertically organized systems of columns.
Abstract: Of the many possible functions of the macaque monkey primary visual cortex (striate cortex, area 17) two are now fairly well understood. First, the incoming information from the lateral geniculate bodies is rearranged so that most cells in the striate cortex respond to specifically oriented line segments, and, second, information originating from the two eyes converges upon single cells. The rearrangement and convergence do not take place immediately, however: in layer IV c, where the bulk of the afferents terminate, virtually all cells have fields with circular symmetry and are strictly monocular, driven from the left eye or from the right, but not both; at subsequent stages, in layers above and below IV c, most cells show orientation specificity, and about half are binocular. In a binocular cell the receptive fields in the two eyes are on corresponding regions in the two retinas and are identical in structure, but one eye is usually more effective than the other in influencing the cell; all shades of ocular dominance are seen. These two functions are strongly reflected in the architecture of the cortex, in that cells with common physiological properties are grouped together in vertically organized systems of columns. In an ocular dominance column all cells respond preferentially to the same eye. By four independent anatomical methods it has been shown that these columns have the

1,407 citations

Journal Article•DOI•
Torsten N. Wiesel1•
14 Oct 1982-Nature
TL;DR: The following is the lecture delivered by the author in Stockholm on 8 December 1981 when he received the Nobel Prize in Medicine, which he shared with Roger Sperry and David H. Hubel.
Abstract: The following is the lecture delivered by the author in Stockholm on 8 December 1981 when he received the Nobel Prize in Medicine, which he shared with Roger Sperry and David H. Hubel The article is published here with permission from the Nobel Foundation and will also be included in the complete volume of Les Prix Nobel en 1981 as well as in the series Nobel Lectures (in English) lished by Elsevier.

846 citations

References
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Journal Article•DOI•
TL;DR: In these experiments the use of monocular deprivation made it possible to compare adjacent geniculate layers, and also to compare the two eyes in their ability to influence cortical cells, so that each animal acted, in a sense, as its own control.
Abstract: IN THE NORMAL CAT OR KITTEN about four-fifths of cells in the striate cortex can be driven by both eyes (3, 4). If, however, one eye of a newborn kitten is sewn shut and the visual cortex recorded from 3 months later, only a small fraction of cells can be driven from the deprived eye (8) . In contrast, many cells in the latera .I geniculate are driven normally from the d ,eprived eye (7 ), suggesting that the abnormality occurs somewhere between geniculate cells and cortex. Since clear receptive-field orientations and directional preferences to movement are seen in cortical cells of newborn visually inexperienced kittens, the deprivation effects presumably represent some sort of disruption of innately determined connections, rather than a failure of postnatal development related to lack of experience. In these experiments the use of monocular deprivation made it possible to compare adjacent geniculate layers, and also to compare the two eyes in their ability to influence cortical cells, so that each animal acted, in a sense, as its own control. The results led us to expect that depriving both eyes for similar periods would lead to an almost total unresponsiveness of cortical cells to stimulation of either eye. That should be so, provided the effects of depriving one eye were independent of whether or not the other eye was simultaneously deprived. It seemed worthwhile to test such an assumption, since any interdependence of the two pathways would be of considerable interest. We accordingly raised kittens with both eyes covered by lid suture, and recorded from the striate cortex when the animals had reached an age of 23-43 months.

1,520 citations

Journal Article•DOI•
TL;DR: Single-unit recordings in the optic tract and lateral geniculate body of kittens in which one eye had been deprived of vision are described, and an anatomical examination of the visual pathways in these animals are examined.
Abstract: THEIMPORTANCEOFNORMALSENSORYSTIMULATION inthedevelopment and maintenance of the nervous system is now generally recognized. In the visual system this problem has usually been approached by examining the effects of sensory deprivation on structure and behavior (see reviews by Hebb (12) and Riesen (28)). An obvious way of extending this work would be to examine electrophysiologically the functional effects of visual deprivation, but such experiments require some knowledge of normal function. During the last 10 years single-cell responses have been examined and receptive-field arrangements compared at several levels in the cat’s visual pathway: in the retina (Zl), the lateral geniculate body (18), and the visual cortex (17, 19). This information provides the necessary background for a study of the immature and the stimulus-deprived visual system. The results of a physiological and anatomical study of the visual pathways in normal. and visually deprived kittens will be presented in a series of three papers. In the present paper we describe single-unit recordings in the optic tract and lateral geniculate body of kittens in which one eye had been deprived of vision, and an anatomical examination of the visual pathways in these animals. The second paper (20) will describe single-unit recordings in the striate cortex of newborn kittens. The final paper (32) will deal with responses of cells in the visual cortex of visually deprived animals.

1,238 citations

Journal Article•DOI•
TL;DR: Receptive fields of geniculate receptive fields resembled those of retinal ganglion cells, having an excitatory ('on') centre and inhibitory preriphery, or reverse, and cells with receptive fields within or near the area centralis tended to have smaller field centres and stronger suppression by the receptive field periphery than cells with their fields situated in more peripheral regions of the retina.
Abstract: : Cells were recorded with tungsten electrodes in the dorsal lateral geniculate body of the cat Receptive fields of these units were mapped out, in the light-adapted state, with small sports of light In their general arrangement geniculate receptive fields resembled those of retinal ganglion cells, having an excitatory ('on') centre and inhibitory ('off') preriphery, or reverse The two portions of a receptive field were mutually antagonistic; the decrease in centre responses cauded by inclusion of peripheral portions of receptive fields was termed peripheral suppression Cells recorded in layers A and B of the lateral geniculate body were driven from the contralateral eye; cells in layer A1 from the ipsilateral eye In penetrations normal to the layers receptive fields of cells in a single layer were close together or superimposed, and from one layer to the next occupied exactly homologous positions in the two retinas Binocular interaction was not observed in any of the cells studied All three layers of the lateral geniculate contained both 'on'-centre and 'off'-centre units Cells in layers A and A1 were similar both in their firing patterns and in average receptive field size Cells in layer B were more sluggish in their responses to light stimuli, and tended to have larger receptive field centres Cells with receptive fields within or near the area centralis tended to have smaller field centres and stronger suppression by the receptive field periphery than cells with their fields situated in more peripheral regions of the retina

771 citations

Journal Article•DOI•
TL;DR: Seven kittens were used, and the various procedures of deprivation and subsequent studies are summarized in Table 1.
Abstract: Seven kittens were used, and the various procedures of deprivation and subsequent studies are summarized in Table 1. In six animals the Iids of one eye were closed for the first 3 months of life. In the recovery period two of these kittens had the deprived eye opened. The other four had the deprived eye opened and the other (previously open) eye was closed. The seventh animal had both eyes closed for 3 months; the right eye was then opened. Recovery periods

670 citations

Journal Article•DOI•

202 citations