Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance

1976 ◽  
Vol 39 (6) ◽  
pp. 1320-1333 ◽  
Author(s):  
P. H. Schiller ◽  
B. L. Finlay ◽  
S. F. Volman

1. Quantitative analyses of orientation specificity and ocular dominance were carried out in striate cortex of the rhesus monkey. 2. Sharpness of orientation selectivity was greater for simple (S type) than for complex (CX type) cells. CX-type cells became more broadly tuned in the deeper cortical layers: S-type cells were equally well tuned throughout the cortex. 3. Sharpness of orientation selectivity for S-type cells was similar at all retinal eccentricities studied (0 degrees - 20 degrees from the fovea):in CX-type cells orientation selectivity decreased slightly with increasing eccentricity. 4. The orientation tuning of binocular cells was similar when mapped separately through each eye. 5. Orientation selectivity and direction selectivity are independent of each other, suggesting that separate neural mechanisms give rise to them. 6. More CX-type cells can be binocularly activated than S-type cells (88% versus 49%). The ocular dominance of S-type cells is similar in all cortical layers: for CX-type cells there is an increase in the number of cells in ocular-dominance category 4 in layers 5 and 6.

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.


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.


2002 ◽  
Vol 88 (4) ◽  
pp. 1933-1940 ◽  
Author(s):  
Chris J. Beaver ◽  
Quentin S. Fischer ◽  
Qinghua Ji ◽  
Nigel W. Daw

We have previously shown that the protein kinase A (PKA) inhibitor, 8-chloroadenosine-3′,5′–monophosphorothioate (Rp-8-Cl-cAMPS), abolishes ocular dominance plasticity in the cat visual cortex. Here we investigate the effect of this inhibitor on orientation selectivity. The inhibitor reduces orientation selectivity in monocularly deprived animals but not in normal animals. In other words, PKA inhibitors by themselves do not affect orientation selectivity, nor does monocular deprivation by itself, but monocular deprivation in combination with a PKA inhibitor does affect orientation selectivity. This result is found for the receptive fields in both deprived and nondeprived eyes. Although there is a tendency for the orientation selectivity in the nondeprived eye to be higher than the orientation selectivity in the deprived eye, the orientation selectivity in both eyes is considerably less than normal. The result is striking in animals at 4 wk of age. The effect of the monocular deprivation on orientation selectivity is reduced at 6 wk of age and absent at 9 wk of age, while the effect on ocular dominance shifts is less changed in agreement with previous results showing that the critical period for orientation/direction selectivity ends earlier than the critical period for ocular dominance. We conclude that closure of one eye in combination with inhibition of PKA reduces orientation selectivity during the period that orientation selectivity is still mutable and that the reduction in orientation selectivity is transferred to the nondeprived eye.


1989 ◽  
Vol 2 (1) ◽  
pp. 41-55 ◽  
Author(s):  
A. B. Bonds

AbstractMechanisms supporting orientation selectivity of cat striate cortical cells were studied by stimulation with two superimposed sine-wave gratings of different orientations. One grating (base) generated a discharge of known amplitude which could be modified by the second grating (mask). Masks presented at nonoptimal orientations usually reduced the base-generated response, but the degree of reduction varied widely between cells. Cells with narrow orientation tuning tended to be more susceptible to mask presence than broadly tuned cells; similarly, simple cells generally showed more response reduction than did complex cells.The base and mask stimuli were drifted at different temporal frequencies which, in simple cells, permitted the identification of individual response components from each stimulus. This revealed that the reduction of the base response by the mask usually did not vary regularly with mask orientation, although response facilitation from the mask was orientation selective. In some sharply tuned simple cells, response reduction had clear local maxima near the limits of the cell's orientation-tuning function.Response reduction resulted from a nearly pure rightward shift of the response versus log contrast function. The lowest mask contrast yielding reduction was within 0.1–0.3 log unit of the lowest contrast effective for excitation.The temporal-frequency bandpass of the response-reduction mechanism resembled that of most cortical cells. The spatial-frequency bandpass was much broader than is typical for single cortical cells, spanning essentially the entire visual range of the cat.These findings are compatible with a model in which weak intrinsic orientation-selective excitation is enhanced in two stages: (1) control of threshold by nonorientation-selective inhibition that is continuously dependent on stimulus contrast; and (2) in the more narrowly tuned cells, orientation-selective inhibition that has local maxima serving to increase the slope of the orientation-tuning function.


1998 ◽  
Vol 15 (1) ◽  
pp. 177-196 ◽  
Author(s):  
J. MCLEAN ◽  
L.A. PALMER

We have utilized an associative conditioning paradigm to induce changes in the receptive field (RF) properties of neurons in the adult cat striate cortex. During conditioning, the presentation of particular visual stimuli were repeatedly paired with the iontophoretic application of either GABA or glutamate to control postsynaptic firing rates. Similar paradigms have been used in kitten visual cortex to alter RF properties (Fregnac et al., 1988, 1992; Greuel et al., 1988; Shulz & Fregnac, 1992). Roughly half of the cells that were subjected to conditioning with stimuli differing in orientation were found to have orientation tuning curves that were significantly altered. In general, the modification in orientation tuning was not accompanied by a shift in preferred orientation, but rather, responsiveness to stimuli at or near the positively reinforced orientation was increased relative to controls, and responsiveness to stimuli at or near the negatively reinforced orientation was decreased relative to controls. A similar proportion of cells that were subjected to conditioning with stimuli differing in spatial phase were found to have spatial-phase tuning curves that were significantly modified. Conditioning stimuli typically differed by 90 deg in spatial phase, but modifications in spatial-phase angle were generally 30–40 deg. An interesting phenomenon we encountered was that during conditioning, cells often developed a modulated response to counterphased grating stimuli presented at the null spatial phase. We present an example of a simple cell for which the shift in preferred spatial phase measured with counterphased grating stimuli was comparable to the shift in spatial phase computed from a one-dimensional Gabor fit of the space-time RF profile. One of ten cells tested had a significant change in direction selectivity following associative conditioning. The specific and predictable modifications of RF properties induced by our associative conditioning procedure demonstrate the ability of mature visual cortical neurons to alter their integrative properties. Our results lend further support to models of synaptic plasticity where temporal correlations between presynaptic and postsynaptic activity levels control the efficiency of transmission at existing synapses, and to the idea that the mature visual cortex is, in some sense, dynamically organized.


1976 ◽  
Vol 39 (6) ◽  
pp. 1362-1374 ◽  
Author(s):  
P. H. Schiller ◽  
B. L. Finlay ◽  
S. F. Volman

1. Several statistical analyses were performed on 205 S-type and CX-type cells which had been completely analyzed on 12 response variables: orientation tuning, end stopping, spontaneous activity, response variability, direction selectivity, contrast selectivity for flashed or moving stimuli, selectivity for interaction of contrast and direction of stimulus movement, spatial-frequency selectivity, spatial separation of subfields responding to light increment of light decrement, sustained/transient response to flash, receptive-field size, and ocular dominance. 2. Correlation of these variables showed that within any cell group, these response variables vary independently. 3. A multivariate discriminant analysis showed that orientation specificity, receptive-field size, interaction of direction and contrast specificity ocular dominance, and spontaneous activity, taken together can adequately assign cells into the S-type or CX-type subgroups. 4. Various models of visual cortex are examined in view of the findings reported here and in the previous papers of this series, which suggest that a) orientation and direction selectivities are produced by separate neural mechanisms, b) there may be hierarchy among simple (S type) cells, and c) complex (CX-type) cells appear to receive a prominent S-type cell input.


1986 ◽  
Vol 56 (4) ◽  
pp. 1062-1073 ◽  
Author(s):  
J. G. Malpeli ◽  
C. Lee ◽  
H. D. Schwark ◽  
T. G. Weyand

Reversible inactivation of individual layers of the cat lateral geniculate and medial interlaminar nuclei was used to investigate the necessary and sufficient inputs for maintaining visually driven activity and receptive field properties in area 17. Neither orientation selectivity nor direction selectivity depends on any individual geniculate layer. We identified two groups of cortical layers on the basis of the pattern of thalamic inputs providing visual driving through the contralateral eye. One group, consisting of layers 4 and 6, has geniculate layer A as its only necessary and sufficient input. The other, consisting of supragranular layers, integrates at least two sufficient thalamic inputs, one of which is layer A. Several major receptive field properties are independently generated in these two groups of layers.


1995 ◽  
Vol 12 (2) ◽  
pp. 309-320 ◽  
Author(s):  
John D. Allison ◽  
Vivien A. Casagrande ◽  
A.B. Bonds

AbstractThe receptive fields of cells in the primary visual cortex (area 17 or V1) show clear orientation selectivity, unlike those of the lateral geniculate nucleus (LGN) cells which provide their visual input. The intrinsic circuitry of V1 cells is believed to be partly responsible for this selectivity. We investigated the influence of ascending projections from neurons in the lower layers (5 and 6) of V1 on the orientation selectivity of single neurons in the upper layers (2, 3, and 4) by reversibly inactivating (“blocking”) lower layer neural activity with iontophoretic application of γ-aminobutyric acid (GABA) while recording from upper layer cells in the prosimian primate, Galago crassicaudatus. During lower layer blocking, the majority (20/28 = 71.4%) of upper layer neurons exhibited a change in the orientation of their preferred stimulus, a reduction in their orientation tuning, and/or an increase in their response amplitude. Twelve (42.9%) neurons exhibited shifts in their preferred orientation averaging 11 (±4) deg. These neurons were located, on average, 272 (±120) μm tangential from the vertical axis of the pipette center. Eleven neurons (39.2%) exhibited an average reduced orientation tuning of 52.5%. Their average location was 230 ± (115) ftm away from the vertical axis of the pipette. Five (17.9%) neurons with average location 145 (±75) firn from the vertical axis exhibited both effects. Two (7.1%) neurons that exhibited significant increases in response amplitude to stimulus angles within 10 deg of the peak excitatory stimulus without changes in orientation selectivity or tuning were located less than 100 μm from the vertical axis. The effects on the orientation tuning of cells were restricted in all cases to within ±30 deg of the preferred stimulus orientation. This suggests that layer blocking affects cells with preferred stimulus orientations similar to those of the recorded neurons. Only cells located within 500 μm tangential to the vertical axis of the injection site exhibited these effects. These results suggest that cells within layers 5 and 6 provide organized, orientation-tuned inhibition that sharpens the orientation tuning of cells in the upper cortical layers within the same, or closely neighboring, cell columns.


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