Functional organization of neurons in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map

1983 ◽  
Vol 49 (4) ◽  
pp. 1051-1072 ◽  
Author(s):  
B. R. Payne ◽  
N. Berman
1976 ◽  
Vol 39 (3) ◽  
pp. 512-533 ◽  
Author(s):  
J. R. Wilson ◽  
S. M. Sherman

1. Receptive-field properties of 214 neurons from cat striate cortex were studied with particular emphasis on: a) classification, b) field size, c) orientation selectivity, d) direction selectivity, e) speed selectivity, and f) ocular dominance. We studied receptive fields located throughtout the visual field, including the monocular segment, to determine how receptivefield properties changed with eccentricity in the visual field.2. We classified 98 cells as "simple," 80 as "complex," 21 as "hypercomplex," and 15 in other categories. The proportion of complex cells relative to simple cells increased monotonically with receptive-field eccenticity.3. Direction selectivity and preferred orientation did not measurably change with eccentricity. Through most of the binocular segment, this was also true for ocular dominance; however, at the edge of the binocular segment, there were more fields dominated by the contralateral eye.4. Cells had larger receptive fields, less orientation selectivity, and higher preferred speeds with increasing eccentricity. However, these changes were considerably more pronounced for complex than for simple cells.5. These data suggest that simple and complex cells analyze different aspects of a visual stimulus, and we provide a hypothesis which suggests that simple cells analyze input typically from one (or a few) geniculate neurons, while complex cells receive input from a larger region of geniculate neurons. On average, this region is invariant with eccentricity and, due to a changing magnification factor, complex fields increase in size with eccentricity much more than do simple cells. For complex cells, computations of this geniculate region transformed to cortical space provide a cortical extent equal to the spread of pyramidal cell basal dendrites.


1982 ◽  
Vol 48 (6) ◽  
pp. 1362-1377 ◽  
Author(s):  
N. Berman ◽  
B. R. Payne ◽  
D. R. Labar ◽  
E. H. Murphy

1. Binocularity and receptive-field type of cortical neurons were assessed relative to the cortical layer in which the neurons were recorded and to receptive-field position in the visual field. 2. Receptive fields were observed up to 2 degrees into the ipsilateral half of the visual field. In the region up to 2 degrees on either side of the vertical meridian, the relative contribution of the ipsilateral eye was reduced. This progression in ocular dominance from ipsilateral to contralateral visual field agrees well with the distribution of X-cells about the nasotemporal division. 3. The region of maximum binocularity in each hemifield was found to be a 12 degree wide vertical strip extending from the vertical meridian to 12 degrees contralateral. In the representation of the central 12 degree strip, most units in all cortical layers were binocular. 4. Low levels of binocularity were observed at a considerable distance before the monocular portion of the visual field was reached. 5. The decrease in binocularity for simple cells occurred closer to the vertical meridian than for complex cells. 6. The proportions of cells classified as simple or complex did not change with position in the visual field. 7. At all locations in the visual field, complex cells showed a higher percentage of binocularity than simple cells. 8. The proportions of two types of simple cells, I and II, and complex cells were variable between cortical layers. Layer IV contained predominantly simple II cells, whereas layer V contained predominantly complex cells. 9. The results are discussed in terms of visual perception and the dynamic pattern of visual stimulation around a moving animal, the optic flow field.


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 form of vertically disposed alternating left-eye and right-eye slabs, which in horizontal section form alternating stripes about 400 μm 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°, 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° 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.


1979 ◽  
Vol 204 (1157) ◽  
pp. 415-434 ◽  

Receptive field position and orientation disparities are both properties of binocularly discharged striate neurons. Receptive field position disparities have been used as a key element in the neural theory for binocular depth discrimination. Since most striate cells in the cat are binocular, these position disparities require that cells immediately adjacent to one another in the cortex should show a random scatter in their monocular receptive field positions. Superimposed on the progressive topographical representation of the visual field on the striate cortex there is experimental evidence for a localized monocular receptive field position scatter. The suggestion is examined that the binocular position disparities are built up out of the two monocular position scatters. An examination of receptive field orientation disparities and their relation to the random variation in the monocular preferred orientations of immediately adjacent striate neurons also leads to the conclusion that binocular orientation disparities are a consequence of the two monocular scatters. As for receptive field position, the local scatter in preferred orientation is superimposed on a progressive representation of orientation over larger areas of the cortex. The representation in the striate cortex of visual field position and of stimulus orientation is examined in relation to the correlation between the disparities in receptive field position and preferred orientation. The role of orientation disparities in binocular vision is reviewed.


1978 ◽  
Vol 41 (2) ◽  
pp. 322-337 ◽  
Author(s):  
D. W. Watkins ◽  
J. R. Wilson ◽  
S. M. Sherman

1. We studied the receptive fields of 171 striate cortical neurons from 17 cats raised with binocular lid suture. Of these, 102 fields were within 10 degrees of the area centralis and the remaining 69 were at least 38 degrees from the vertical meridian. 2. Based on their different response properties, cells were divided into three broad groups: the mappable cells (49%) had clearly defined receptive fields, the unmappable cells (31%) were activated by visual stimuli but had diffuse fields which could not be hand plotted, and the visually inexcitable cells (20%) could not be activated by visual stimuli. Very few (less than or equal to 12% of the total sample) normal simple or complex cells could be found. 3. Orientation selectivity was assessed in these cells. Only 12% displayed orientation selectivity within normal bounds, and these were all mappable cells. None of the unmappable cells had discernible orientation selectivity. 4. Ocular dominance was assessed for 62 of the centrally located receptive fields. Among mappable cells, there was an abnormally low proportion of binocular fields, while no such abnormality was seen for unmappable cells. 5. For 47 of the neurons, average response histograms were compiled for moving stimuli of various parameters in an effort to evoke the maximum discharge or peak response. This peak response was normal for mappable cells but reduced for unmappable cells. 6. We devised a technique for studying potential inhibitory receptive-field zones in these neurons, validated the method in normal striate cortex, and used it to test 20 mappable cells in the lid-sutured cats. None showed the pattern of strong inhibitory side bands seen in normal simple cells, although six showed weak or abnormal inhibitory zones. Interestingly, six of the seven visually inexcitable cells tested by this method had purely inhibitory receptive fields. 7. The effects of binocular suture were essentially identical for the binocular and monocular segments since the cell types and their response properties did not differ between these two areas of cortex. Furthermore, the cortical monocular segments of these cats seemed qualitatively different from the deprived cortical monocular segment after monocular suture. This extends an analogous difference for these cats reported for the monocular segments of the lateral geniculate nucleus. We thus conclude that monocularly and binocularly sutured cats develop by qualitatively different mechanisms. For the former, competition between central synapses related to each eye is a prominent feature of geniculocortical development, whereas, for the latter, such specific forms of geniculocortical development may not obtain.


1986 ◽  
Vol 55 (6) ◽  
pp. 1136-1152 ◽  
Author(s):  
C. L. Baker ◽  
M. S. Cynader

Responses of direction-selective neurons in cat striate cortex (area 17) were studied with flashed-bar stimuli. Spatial parameters of interactions within the receptive field giving rise to direction selectivity and of receptive-field subunits were quantitatively determined for the same cells and correlated. A bar stimulus flashed sequentially at two nearby locations in the receptive field produced direction-selective behavior comparable with that elicited by continuously moving stimuli. Each cell exhibited a characteristic optimal spatial displacement, Dopt, for which responses in the presumed preferred and null directions were maximally distinct. In all cases, Dopt was much smaller than the receptive-field size. The spatial structure of receptive fields in simple cells was studied using single narrow-bar stimuli flashed at different locations in the receptive field. The resulting line-weighting function exhibited alternating regions of ON and OFF responses having a characteristic spatial period or wavelength, lambda. Spatial subunit structure in complex cells was determined by flashing two bars simultaneously in the receptive field. The response as a function of bar separation was again a wavelike function having a spatial wavelength, lambda. Values of the optimal displacement for direction selectivity, Dopt, showed a clear relationship with the spatial wavelength, lambda, for a given unit. Dopt was also correlated to a somewhat lesser degree with receptive-field size. Generally, the ratio of Dopt to lambda was approximately 1/10 to 1/4, in agreement with theoretical predictions by Marr and Poggio. Taken together with the findings of Movshon et al., these results indicate a systematic relationship between Dopt and the spatial frequency of a sinusoidal grating, which is optimal for that cell. Such a relationship is consistent with the results of human psychophysical experiments on apparent motion.


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