Residual Binocular Interactions in the Striate Cortex of Monkeys Reared With Abnormal Binocular Vision

1997 ◽  
Vol 78 (3) ◽  
pp. 1353-1362 ◽  
Author(s):  
Earl L. Smith ◽  
Yuzo M. Chino ◽  
Jinren Ni ◽  
Han Cheng ◽  
M.L.J. Crawford ◽  
...  

Smith, Earl L., III, Yuzo M. Chino, Jinren Ni, Han Cheng, M.L.J. Crawford, and Ronald S. Harwerth. Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. J. Neurophysiol. 78: 1353–1362, 1997. We investigated the nature of residual binocular interactions in the striate cortex (V1) of monkey models for the two most common causes of visual dysfunction in young children, specifically anisometropia and strabismus. Infant rhesus monkeys were raised wearing either anisometropic spectacle lenses that optically defocused one eye or ophthalmic prisms that optically produced diplopia and binocular confusion. Earlier psychophysical investigations had demonstrated that all subjects exhibited permanent binocular vision deficits and, in some cases, amblyopia. When the monkeys were adults, the responses of individual V1 neurons were studied with the use of microelectrode recording techniques while the animals were anesthetized and paralyzed. The manner in which the signals from the two eyes were combined in individual cells was investigated by dichoptically stimulating both eyes simultaneously with drifting sine wave gratings. In both lens- and prism-reared monkeys, fewer neurons had balanced ocular dominances and greater numbers of neurons were excited by only one eye. However, many neurons that appeared to be monocular exhibited clear binocular interactions during dichoptic stimulation. For the surviving binocular neurons, the maximum binocular response amplitudes were lower than normal; fewer neurons, particularly complex cells, were sensitive to relative interocular spatial phase disparities; and the remaining disparity-sensitive neurons exhibited lower degrees of binocular interaction. In prism-reared monkeys, an unusually high proportion of complex cells exhibited binocular suppression during dichoptic stimulation. Binocular contrast summation experiments showed that for both cooperative and antagonistic binocular interactions, contrast signals from the two eyes were combined by individual neurons in a normal linear fashion in both lens- and prism-reared monkeys. The observed binocular deficits appear to reflect a reduction in functional inputs from one eye and/or spatial imprecision in the monocular receptive fields rather than an aberrant form of binocular interaction. In the prism-reared monkeys, the predominance of suppression suggests that inhibitory connections were, however, less susceptible to diplopia and confusion than excitatory connections. Overall, there were many parallels between V1 physiology in our monkey models and the residual vision of humans with anisometropia or strabismus.

1997 ◽  
Vol 78 (1) ◽  
pp. 366-382 ◽  
Author(s):  
Earl L. Smith ◽  
Yuzo Chino ◽  
Jinren Ni ◽  
Han Cheng

Smith, Earl L., III, Yuzo Chino, Jinren Ni, and Han Cheng. Binocular combination of contrast signals by striate cortical neurons in the monkey. J. Neurophysiol. 78: 366–382, 1997. With the use of microelectrode recording techniques, we investigated how the contrast signals from the two eyes are combined in individual cortical neurons in the striate cortex of anesthetized and paralyzed macaque monkeys. For a given neuron, the optimal spatial frequency, orientation, and direction of drift for sine wave grating stimuli were determined for each eye. The cell's disparity tuning characteristics were determined by measuring responses as a function of the relative interocular spatial phase of dichoptic stimuli that consisted of the optimal monocular gratings. Binocular contrast summation was then investigated by measuring contrast response functions for optimal dichoptic grating pairs that had left- to right-eye interocular contrast ratios that varied from 0.1 to 10. The goal was to determine the left- and right-eye contrast components required to produce a criterion threshold response. For all functional classes of cortical neurons and for both cooperative and antagonistic binocular interactions, there was a linear relationship between the left- and right-eye contrast components required to produce a threshold response. Thus, for example for cooperative binocular interactions, a reduction in contrast to one eye was counterbalanced by an equivalent increase in contrast to the other eye. These results showed that in simple cells and phase-specific complex cells, the contrast signals from the two eyes were linearly combined at the subunit level before nonlinear rectification. In non-phase-specific complex cells, the linear binocular convergence of contrast signals could have taken place either before or after the rectification process, but before spike generation. In addition, for simple cells, vector analysis of spatial summation showed that the inputs from the two eyes were also combined in a linear manner before nonlinear spike-generating mechanisms. Thus simple cells showed linear spatial summation not only within and between subregions in a given receptive field, but also between the left- and right-eye receptive fields. Overall, the results show that the effectiveness of a stimulus in producing a response reflects interocular differences in the relative balance of inputs to a given cell, however, the eye of origin of a light-evoked signal has no specific consequence.


1999 ◽  
Vol 82 (2) ◽  
pp. 909-924 ◽  
Author(s):  
Akiyuki Anzai ◽  
Izumi Ohzawa ◽  
Ralph D. Freeman

Complex cells in the striate cortex exhibit extensive spatiotemporal nonlinearities, presumably due to a convergence of various subunits. Because these subunits essentially determine many aspects of a complex cell receptive field (RF), such as tuning for orientation, spatial frequency, and binocular disparity, examination of the RF properties of subunits is important for understanding functional roles of complex cells. Although monocular aspects of these subunits have been studied, little is known about their binocular properties. Using a sophisticated RF mapping technique that employs binary m-sequences, we have examined binocular interactions exhibited by complex cells in the cat’s striate cortex and the binocular RF properties of their underlying functional subunits. We find that binocular interaction RFs of complex cells exhibit subregions that are elongated along the frontoparallel axis at different binocular disparities. Therefore responses of complex cells are largely independent of monocular stimulus position or phase as long as the binocular disparity of the stimulus is kept constant. The binocular interaction RF is well described by a sum of binocular interaction RFs of underlying functional subunits, which exhibit simple cell-like RFs and a preference for different monocular phases but the same binocular disparity. For more than half of the complex cells examined, subunits of each cell are consistent with the characteristics specified by an energy model, with respect to the number of subunits as well as relationships between the subunit properties. Subunits exhibit RF binocular disparities that are largely consistent with a phase mechanism for encoding binocular disparity. These results indicate that binocular interactions of complex cells are derived from simple cell-like subunits, which exhibit multiplicative binocular interactions. Therefore binocular interactions of complex cells are also multiplicative. This suggests that complex cells compute something analogous to an interocular cross-correlation of images for a local region of visual space. The result of this computation can be used for solving the stereo correspondence problem.


1996 ◽  
Vol 13 (3) ◽  
pp. 559-566 ◽  
Author(s):  
John D. Allison ◽  
J. F. Kabara ◽  
R. K. Snider ◽  
V. A. Casagrande ◽  
A. B. Bonds

AbstractBlocking GABAA-receptor-mediated inhibition reduces the selectivity of striate cortical neurons for the orientation of a light bar primarily by reducing the selectivity of their onset transient (initial 200 ms) response. Blocking GABAB-receptor-mediated inhibition with phaclofen, however, is not reported to reduce the orientation selectivity of these neurons when it is measured with a light bar. We hypothesized that blocking GABAB-receptor-mediated inhibition would instead affect the orientation selectivity of cortical neurons by reducing the selectivity of their sustained response to a prolonged stimulus. To test this hypothesis, we stimulated 21 striate cortical neurons with drifting sine-wave gratings and measured their orientation selectivity before, during, and after iontophoretic injection of 2-hydroxy-saclofen (2-OH-S), a selective GABAB-receptor antagonist. 2-OH-S reduced the orientation selectivity of six of eight simple cells by an average of 28.8 (± 13.2)% and reduced the orientation selectivity of eight of 13 complex cells by an average of 32.3 (± 27.4)%. As predicted, 2-OH-S reduced the orientation selectivity of the neurons' sustained response, but did not reduce the orientation selectivity of their onset transient response. 2-OH-S also increased the length of spike “bursts” (two or more spikes with interspike intervals ≤ 8 ms) and eliminated the orientation selectivity of these bursts for six cells. These results are the first demonstration of a functional role for GABAB receptors in visual cortex and support the hypothesis that two GABA-mediated inhibitory mechanisms, one fast and the other slow, operate within the striate cortex to shape the response properties of individual neurons.


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.


2000 ◽  
Vol 84 (5) ◽  
pp. 2529-2540 ◽  
Author(s):  
Douglas R. W. Wylie ◽  
Nathan A. Crowder

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion. Previous studies have shown that LM neurons have large receptive fields in the contralateral eye, are excited in response to largefield stimuli moving in a particular (preferred) direction, and are inhibited in response to motion in the opposite (anti-preferred) direction. We investigated the responses of LM neurons to sine wave gratings of varying spatial and temporal frequency drifting in the preferred and anti-preferred directions. The LM neurons fell into two categories. “Fast” neurons were maximally excited by gratings of low spatial [0.03–0.25 cycles/° (cpd)] and mid-high temporal frequencies (0.5–16 Hz). “Slow” neurons were maximally excited by gratings of high spatial (0.35–2 cpd) and low-mid temporal frequencies (0.125–2 Hz). Of the slow neurons, all but one preferred forward (temporal to nasal) motion. The fast group included neurons that preferred forward, backward, upward, and downward motion. For most cells (81%), the spatial and temporal frequency that elicited maximal excitation to motion in the preferred direction did not coincide with the spatial and temporal frequency that elicited maximal inhibition to gratings moving in the anti-preferred direction. With respect to motion in the anti-preferred direction, a substantial proportion of the LM neurons (32%) showed bi-directional responses. That is, the spatiotemporal plots contained domains of excitation in addition to the region of inhibition. Neurons tuned to stimulus velocity across different spatial frequency were rare (5%), but some neurons (39%) were tuned to temporal frequency. These results are discussed in relation to previous studies of the responses of neurons in the accessory optic system and pretectum to drifting gratings and other largefield stimuli.


1991 ◽  
Vol 66 (2) ◽  
pp. 379-389 ◽  
Author(s):  
T. J. Gawne ◽  
B. J. Richmond ◽  
L. M. Optican

1. Although neurons within the visual system are often described in terms of their responses to particular patterns such as bars and edges, they are actually sensitive to many different stimulus features, such as the luminances making up the patterns and the duration of presentation. Many different combinations of stimulus parameters can result in the same neuronal response, raising the problem of how the nervous system can extract information about visual stimuli from such inherently ambiguous responses. It has been shown that complex cells transmit significant amounts of information in the temporal modulation of their responses, raising the possibility that different stimulus parameters are encoded in different aspects of the response. To find out how much information is actually available about individual stimulus parameters, we examined the interactions among three stimulus parameters in the temporally modulated responses of striate cortical complex cells. 2. Sixteen black and white patterns were presented to two awake monkeys at each of four luminance-combinations and five durations, giving a total of 320 unique stimuli. Complex cells were recorded in layers 2 and 3 of striate cortex, with the stimuli centered on the receptive fields as determined by mapping with black and white bars. 3. An analysis of variance (ANOVA) was applied to these data with the three stimulus parameters of pattern, the luminance-combinations, and duration as the independent variables. The ANOVA was repeated with the magnitude and three different aspects of the temporal modulation of the response as the dependent variables. For the 19 neurons studied, many of the interactions between the different stimulus parameters were statistically significant. For some response measures the interactions accounted for more than one-half of the total response variance. 4. We also analyzed the stimulus-response relationships with the use of information theoretical techniques. We defined input codes on the basis of each stimulus parameter alone, as well as their combinations, and output codes on the basis of response strength, and on three measures of temporal modulation, also taken individually and together. Transmitted information was greatest when the response of a neuron was interpreted as a temporally modulated message about combinations of all three stimulus parameters. The interaction terms of the ANOVA suggest that the response of a complex cell can only be interpreted as a message about combinations of all three stimulus parameters.(ABSTRACT TRUNCATED AT 400 WORDS)


2007 ◽  
Vol 97 (4) ◽  
pp. 3070-3081 ◽  
Author(s):  
Gregory D. Horwitz ◽  
E. J. Chichilnisky ◽  
Thomas D. Albright

Rules by which V1 neurons combine signals originating in the cone photoreceptors are poorly understood. We measured cone inputs to V1 neurons in awake, fixating monkeys with white-noise analysis techniques that reveal properties of light responses not revealed by purely linear models used in previous studies. Simple cells were studied by spike-triggered averaging that is robust to static nonlinearities in spike generation. This analysis revealed, among heterogeneously tuned neurons, two relatively discrete categories: one with opponent L- and M-cone weights and another with nonopponent cone weights. Complex cells were studied by spike-triggered covariance, which identifies features in the stimulus sequence that trigger spikes in neurons with receptive fields containing multiple linear subunits that combine nonlinearly. All complex cells responded to nonopponent stimulus modulations. Although some complex cells responded to cone-opponent stimulus modulations too, none exhibited the pure opponent sensitivity observed in many simple cells. These results extend the findings on distinctions between simple and complex cell chromatic tuning observed in previous studies in anesthetized monkeys.


1995 ◽  
Vol 74 (3) ◽  
pp. 1271-1286 ◽  
Author(s):  
C. Casanova ◽  
T. Savard ◽  
J. P. Nordmann ◽  
S. Molotchnikoff ◽  
K. Minville

1. Whether complex (C) cells are the only truly texture-sensitive units in the cat's primary visual cortex remains controversial. In view of the strong physiological significance of having putatively only one class of cells sensitive to visual noise in the striate cortex, we reinvestigated this issue. Sensitivities of simple (S) and C cells to noise were quantitatively studied and compared in order to clearly document the response properties of cells in the striate cortex to visual noise and to establish whether one can unequivocally segregate S from C cells on the basis of those specific properties. 2. Receptive fields were stimulated with all relevant stimuli, i.e., drifting sine-wave gratings, electronically generated noise pattern of 256 x 256 elements (ratio 1:1 of dark and light elements), and flashing and moving bars (both bright and dark). 3. A total of 60 S cells out of 85 (70.6%) and 90 C cells out of 101 (81.8%) responded to the motion of visual noise. Responses of most C cells were sustained, i.e., their discharge rate was maintained at a constant level throughout presentation of the stimulus. On the other hand, responses of the majority of S cells were characterized by several bursts of discharges. On average, optimal firing rates were greater for gratings than for noise. 4. For practically all cells, responses to noise varied as a function of direction of motion. The mean direction bandwidths were, respectively, 43 +/- 24 degrees and 48 +/- 23 degrees (mean +/- SD) for S and C cells. In both groups, neurons were more broadly tuned for the direction of noise than that of gratings (t-test, P < 0.001). We rarely observed bimodal tuning curves for noise, with each peak lying on either side of the orientation curve. These results could be expected if one considers texture stimuli not in the space domain (as dot patterns) but in the frequency domain, i.e., patterns containing all spatial frequencies and orientations. 5. In general, the direction indexes of S and C cells were similar whether they were stimulated by drifting noise or gratings. S cells had a slight tendency to be more direction selective for noise than for gratings. 6. For all S and C cells tested, responses to noise varied as a function of drift velocity. The mean optimal velocity was 12.9 and 10.2 degrees/s for S and C cells, respectively (t-test, P > 0.05). Most cells were band-pass with mean bandwidths of 2.2 and 2.7 octaves for S and C cells, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)


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