Projection into the visual field of ocular dominance columns in macaque monkey.
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Biomedical subjects
Publications and source records attributed to D H Hubel.
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In adult mice of the C57BL/6J strain the projection of the visual field was systematically mapped under direct vision. As in other vertebrate species the nasal (anterior) field projected anterolaterally, and the inferior field posterolaterally. Values of magnification-1 (m-1, or degrees of visual field per millimeter tectal surface) were calculated over most of the tectum, for measurements in the coronal and sagittal planes. Whereas m-1 was fairly constant for measurement pairs in sagittal planes, for coronal planes there was a rather large, elongated, horizontally oriented area in the upper field of vision within which m-1 was smaller than elsewhere. In this area m-1 was anisotropic, with a ratio of almost 2:1 between sagittal and coronal planes. In a previously study we had observed that many cells recorded in deeper tectal layers responded to somatosensory stimulation, with whiskers especially conspicuous. In a given penetration perpendicular to the tectal surface, somatosensory receptive fields recorded in the deeper tectum were always concerned with that group of whiskers or with those parts of the body that crossed the regions of visual field represented in the superficial layers directly above. Given this information on the visual coordinates associated with certain somatosensory fields, the detailed mapping of the visual field onto the tectum made it possible to prepare a map of the somatosensory projection on the tectum. The resulting representation differed markedly from maps described for the classic somatosensory pathway. In the tectum the somatosensory map was dictated by the visual-field projection rather than by the peripheral tactile innervation density. Whiskers were thus featured much more prominently in the tectum, and structures close to the eye, such as the pinna and cheek, receive more representation than the tail or hindpaws.
The distribution of retinotectal projections was studied in 4 macaque monkeys by examining the tectum autoradiographically 3-21 days after eye injection with radioactive proline or a proline-fucose mixture. Contrary to previous reports the optic fibers project to all regions of the tectum including a relatively sparse but nevertheless very clear projection to the anterolateral one-third, where the fovea is represented. Here the terminals were distributed within the superficial grey layer of the tectum at a depth extending from about 50 mum to 125 mum and in a patchy fashion, with a tendency to aggregation in clumps 0.1-0.5 mm wide from one or other eye. Further posteromedially, corresponding to more peripheral retinal regions, the input from the contralateral eye became more continuous superficially, with tongues extending more deeply in the superficial grey, apparently enclosing clumps of ipsilateral terminals. These deeper ipsilateral clumps occupied a rather well defined layer extending in depth from about 100 mum to about 175 mum. Still further posteromedially, in the temporal crescent representation, only the continuously distributed label from the contralateral eye was found. Continuous label was also seen in the optic disc region on the ipsilateral side; on the corresponding area contralaterally, label was absent. Both ipsilaterally and contralaterally, the pattern of input was roughly symmetrical about the representation of the horizontal meridian, which ran from anterolateral to posteromedial. The regional aggregations of input from one or other eye were to some extent reflected physiologically in a regional variation in eye dominance, though this was perhaps less than might have been expected from the marked heterogeneity of the inputs.
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A pattern of alternating dark and pale bands was observed in the striate cortex of the macaque monkey. The bands, which ran parallel to the surface, were seen in tangential sections stained with a reduced silver method for normal fibers and were most clear in layer 4C alpha, immediately deep to the line of Gennari. The dark bands were about 300 mu wide and showed blind endings and bifurcations. The light bands were about 50 mu wide and did not branch or terminate within area 17. Because the dark bands were similar in width to the bands of terminal degeneration which have been shown to result from single-layer lesions of the lateral geniculate body, it seemed possible that they corresponded to ocular dominance columns. To test this idea, the boundaries of ocular dominance columns were marked in a physiological experiment: tangential electrode penetrations were made in an anesthetized monkey and, as the electrode was advanced horizontally in the fourth layer, the eye preference of single units and of the background activity was monitored. Small electrolytic lesions were placed at the points where a change in eye preference occurred. The brain was subsequently fixed, sectioned tangentially and stained with the silver method. All the lesions--total of 12 --fell directly on the pale bands. Moreover, the electrode had not passed over any pale bands without a lesion being placed. It was concluded that the dark bands do correspond to single ocular dominance columns and the pale bands to the boundaries between columns. The banding appearance is due to a greater density of tangential fibers within columns than at the borders of columns. These tangential fibers are in part the preterminal arborizations of geniculocortical axons, since some of them have been shown to degenerate after geniculate lesions. The ocular dominance columns were mapped for most of the striate cortex, using serial tangential sections stained with the silver method. The overall pattern was ,imilar in several monkeys, though the details of the branching arrangements varied from animal to animal. The columns met the 17-18 border at right angles. On the outer surface of the hemisphere the columns converged from the 17-18 border, turned medially with repeated fusions of columns, and streamed over the lip of the calcarine fissure. In the roof of the fissure they met a second system of columns oriented parasagittally. In terms of the visual field, the columns ran roughly horizontally for the central 10 degrees of the field, and circumferentially beyond that. The columns were not mapped in the stem of the fissure, the area corresponding to the far periphery of the field. The constancy of column width across the cortex probably allows a functional matching between ocular-dominance and orientation columns.
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The superior colliculus was studied in anesthetized mice by recording from single cells and from unit clusters. The topographic representation of the visual filed was similar to what has been found in other mammals, with the temporal part of the contralateral visual field projecting posteriorly and the inferior visual field projecting laterally. At the anterior margin of the tectum receptive fields recorded through the contralateral eye and invaded the ipsilateral visual hemifield for up to 35 degrees, suggesting that the entire visual field through one eye is represented on the contralateral superior colliculus. Cells located closest to the tectal surface had relatively small receptive fields, averaging 9 degrees in center diameter; field sizes increased steadily with depth. The prevailing cell type in the stratum zonal and superficial gray responded best to a small dark or light object of any shape moved slowly through the receptive-field center or to turning a small stationary spot on or off. Large objects or diffuse light were usually much less effective. Less than one-quarter of superficial layer cells showed directional selectivity to a moving object, the majority of these favoring up and nasal movement. The chief visual cell type in the stratum opticum and upper part of the intermediate gray resembled in the newness neurons described for many other vertebrates: they had large receptive fields and responded best to up and nasal movement of a small dark or light object, whose optimal size was similar to the optimum for upper-layer cells. If the same part of the receptive field was repeatedly stimulated there was a marked tendency to habituate. Only very few cels responded to the ipsilateral eye. Intermixed with visual cells in the upper part of the intermediate gray were cells that responded to somatosensory or auditory stimuli. Here bimodal and trimodal cells were also seen. In deeper layers somatosensory and auditory modalities tended to take over. These two modalities were not segregated into sublayers but rather seemed to be arranged in clusters. Responses to somatosensory and auditory stimuli were brisk, showing little habituation to repeated stimulation.
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1. Guillery has recently shown that the Siamese cat has a grossly abnormal lateral geniculate body. His anatomical study suggested that certain fibres originating in the temporal retina of each eye cross in the chiasm instead of remaining uncrossed. They thus reach the wrong hemispheres, but in the geniculate they terminate in the regions that the missing fibres from the ipsilateral eye would normally have occupied. The result is that each hemisphere receives an input from parts of the ipsilateral field of vision, this input being entirely from the opposite eye. The purpose of the present work was to study the physiological consequences of this aberrant projection, in the lateral geniculate body and visual cortex.2. Single-cell recordings from the lateral geniculate body confirmed the presence of projections from the ipsilateral visual field of the contralateral eye. The part of layer A(1) receiving these projections was arranged so that the receptive fields of the cells were situated at about the same horizontal level and at the same distance from the vertical meridian as the fields of cells in the layers above and below (layers A and B), but were in the ipsilateral visual field instead of the contralateral. They thus occupied a region directly across the mid line from their normal position.3. In the cortex of all animals studied, we found a systematic representation of part of the ipsilateral visual field, inserted between the usual contralateral representations in areas 17 and 18. When the visual cortex was crossed from medial to lateral the corresponding region of visual field moved from the contralateral periphery to the mid line, and then into the ipsilateral field for 20 degrees . The movement then reversed, with a return to the mid line and a steady progression out into the contralateral field. The entire double representation was, with some possible exceptions, a continuous one. The point of reversal occurred at or near the 17-18 boundary, as judged histologically, and this boundary was in about the same position as in ordinary cats.4. Cells in the part of the cortex representing the ipsilateral fields had normal receptive fields, simple, complex, or hypercomplex. These fields tended to be larger than those in corresponding parts of the contralateral visual fields. Receptive-field size varied with distance from the area centralis, just as it does in the normal cat, so that cells with the smallest fields, in the area centralis projection, were situated some distance from the 17-18 border.5. Projections originating from the first 20 degrees from the midvertical in both visual half-fields had their origin entirely in the contralateral eye, as would be expected from the abnormal crossing at the chiasm. Beyond this visual-field region, and out as far as the temporal crescents, there were projections from both eyes, but we found no individual cells with input from the two eyes. The cells were aggregated, with some groups of cells driven by one eye and some by the other.6. From previous work it is known that ordinary cats raised with squint show a decline in the proportion of cells that can be driven binocularly, whereas animals raised with both eyes closed show little or no decline. A Siamese cat raised with both eyes closed had binocular cells in the regions of 17 and 18 subserving the peripheral visual fields, suggesting that the absence of binocular cells seen in the other Siamese cats was indeed secondary to the squint.7. In two Siamese cats there were suggestions of an entirely different projection pattern, superimposed upon that described above. In the parts of 17 and 18 otherwise entirely devoted to the contralateral visual field, we observed groups of cells with receptive fields in the ipsilateral field of vision. The electrode would pass from a region where cells were driven from some part of the contralateral visual field, to regions in which they were driven from a part of the ipsilateral field directly opposite, across the vertical mid line. The borders of these groups were not necessarily sharp, for in places there was mixing of the two groups of cells, and a few cells had input from two discrete regions located opposite one another on either side of the vertical mid line. The two receptive-field components of such cells were identical, in terms of orientation, optimum direction of movement, and complexity. Stimulation of the two regions gave a better response than was produced from either one alone, and the relative effectiveness of the two varied from cell to cell. These cells thus behaved in a way strikingly reminiscent of binocular cells in common cats.8. The apparent existence of two competing mechanisms for determining the projection of visual afferents to the cortex suggests that a number of factors may cooperate in guiding development. There seems, furthermore, not to be a detailed cell-to-cell specificity of geniculocortical connexions, but rather a tendency to topographic order and continuity, with one part of a given area such as 17 able to substitute for another. Whether or not these tentative interpretations are ultimately proved correct, it seems clear that this type of genetic anomaly has potential usefulness for understanding mechanisms of development of the nervous system.
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1. Kittens were visually deprived by suturing the lids of the right eye for various periods of time at different ages. Recordings were subsequently made from the striate cortex, and responses from the two eyes compared. As previously reported, monocular eye closure during the first few months of life causes a sharp decline in the number of cells that can be influenced by the previously closed eye.2. Susceptibility to the effects of eye closure begins suddenly near the start of the fourth week, remains high until some time between the sixth and eighth weeks, and then declines, disappearing finally around the end of the third month. Monocular closure for over a year in an adult cat produces no detectable effects.3. During the period of high susceptibility in the fourth and fifth weeks eye closure for as little as 3-4 days leads to a sharp decline in the number of cells that can be driven from both eyes, as well as an over-all decline in the relative influence of the previously closed eye. A 6-day closure is enough to give a reduction in the number of cells that can be driven by the closed eye to a fraction of the normal. The physiological picture is similar to that following a 3-month monocular deprivation from birth, in which the proportion of cells the eye can influence drops from 85 to about 7%.4. Cells of the lateral geniculate receiving input from a deprived eye are noticeably smaller and paler to Nissl stain following 3 or 6 days' deprivation during the fourth week.5. Following 3 months of monocular deprivation, opening the eye for up to 5 yr produces only a very limited recovery in the cortical physiology, and no obvious recovery of the geniculate atrophy, even though behaviourally there is some return of vision in the deprived eye. Closing the normal eye, though necessary for behavioural recovery, has no detectable effect on the cortical physiology. The amount of possible recovery in the striate cortex is probably no greater if the period of eye closure is limited to weeks, but after a 5-week closure there is a definite enhancement of the recovery, even though it is far from complete.