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Mechanisms underlying cross-orientation suppression in cat visual cortex

Nature Neuroscience volume 9, pages 552–561 (2006)Cite this article

Abstract

In simple cells of the cat primary visual cortex, null-oriented stimuli, which by themselves evoke no response, can completely suppress the spiking response to optimally oriented stimuli. This cross-orientation suppression has been interpreted as evidence for cross-orientation inhibition: synaptic inhibition among cortical cells with different preferred orientations. In intracellular recordings from simple cells, however, we found that cross-oriented stimuli suppressed, rather than enhanced, synaptic inhibition and, at the same time, suppressed synaptic excitation. Much of the suppression of excitation could be accounted for by the behavior of geniculate relay cells: contrast saturation and rectification in relay cell responses, when applied to a linear feed-forward model, predicted cross-orientation suppression of the modulation (F1) component of excitation evoked in simple cells. In addition, we found that the suppression of the spike output of simple cells was almost twice the suppression of their synaptic inputs. Thus, cross-orientation suppression, like orientation selectivity, is strongly amplified by threshold.

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Figure 1: Cross-orientation suppression in simple cells of primary visual cortex.
Figure 2: A summary of cross-orientation effects in the population.
Figure 3: Estimates of excitatory and inhibitory conductance evoked by grating and plaid stimuli.
Figure 4: Two feed-forward models of a simple cell and its responses to grating and plaid stimuli.
Figure 5: A direct comparison of the simple cell input predicted by the nonlinear model in Figure 4c.
Figure 6: The input to a model simple cell derived from the recorded responses of a single geniculate relay cell.
Figure 7: Magnitude of cross-orientation suppression recorded in simple cells and derived from the feed-forward model.
Figure 8: Mask-induced shifts in the contrast response curves.

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Acknowledgements

We are grateful to M.P. Stryker and J.A. Movshon for comments on the manuscript. We also thank J. Hanover for helpful discussions. Supported by grants from the US National Institutes of Health (EY-014499 and EY-04726).

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Authors and Affiliations

  1. Department of Neurobiology and Physiology, Northwestern University, 2145 North Sheridan Drive, Evanston, 60208, Illinois, USA

    Nicholas J Priebe & David Ferster

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Correspondence to David Ferster.

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Supplementary information

Supplementary Fig. 1

Supplementary Figure 1 is a companion to Figure 1 of the paper, providing an additional example of cross-orientation suppression of membrane potential and firing rate in a second cortical simple cell. (PDF 419 kb)

Supplementary Fig. 2

Supplementary Figure 2 is a companion to Figure 2a of the paper. (PDF 1374 kb)

Supplementary Fig. 3

Identification of cells with direct input from the LGN. (PDF 479 kb)

Supplementary Fig. 4

Supplementary Figure 4 is a companion to Figure 3 of the paper, providing three additional examples of cross-orientation suppression of inhibitory and excitatory synaptic conductance in simple cells. (PDF 3291 kb)

Supplementary Fig. 5

Supplementary Figure 5 shows an additional example of cross-orientation suppression in a feed-forward model of a simple cell. (PDF 786 kb)

Supplementary Fig. 6

One of the free parameters used in creating estimates of the relay cell input to simple cells is the aspect ratio of the modeled simple cell subfield. (PDF 826 kb)

Supplementary Fig. 7

Relay responses to plaids with different mask temporal frequencies. (PDF 719 kb)

Supplementary Video 1

The blue mask approximates one subregion of the receptive field of a simple cell, and helps the eye discern how the luminance modulation differs in different points within of the subregion. Test: The amplitude and phase of the contrast modulation are identical in every portion of the receptive field. Mask: The amplitude of the contrast modulation is identical in every portion of the “receptive field”, but temporal phase differs. Plaid: Both the phase and amplitude of the modulation varies across the receptive field. In the outermost windows where the peaks and troughs of the constituent gratings overlap, the contrast modulation is 64%, or double the contrast of the constituent gratings. In the center window, there is a null point where the luminance is nearly unvarying (effective contrast = 0%). (AVI 786 kb)

Supplementary Video 2

One subfield of a simple cell is shown, consisting of the input from 9 ON-center relay cells. The centers of the relay cell receptive fields are shown as circles. The instantaneous spike rate of each relay cell is shown by the color-coded point in each of the graphs below. The synaptic input to the simple from each relay cell is taken to be proportional to the relay cell's spike rate. The scaled sum (mean) of all 9 inputs is shown as the while horizontal line in each graph. In the linear model (middle row), the spike rate of each relay cell is proportional to the luminance of the stimulus, measured relative to the mean luminance. In order to preserve perfect linearity, the spike rate is allowed to become negative. Note that the input to the simple cell(horizontal white line) is identical for the test stimulus and the plaid. In the nonlinear model (bottom row), the spike rate of each relay cell undergoes saturation with a semisaturation constant of 25% contrast, and the firing rate is not allowed to go below 0 (rectification). With both test and mask contrast at 32% contrast, the cross-orientation suppression is subtle, but clearly visible: The amplitude of the modulation of the simple cell's input (horizontal white line) is smaller for the plaid than it is for the test grating. (AVI 887 kb)

Supplementary Video 3

Unlike the Plaid made of two 32%-contrast gratings, there is no null point. The outermost windows, however, experience the highest contrast, and the center window the lowest contrast modulation, and these modulations are out of phase with one another. (AVI 742 kb)

Supplementary Video 4

One subfield of a simple cell is shown, consisting of the input from 9 ON-center relay cells. The centers of the relay cell receptive fields are shown as circles. The instantaneous spike rate of each relay cell is shown by the color-coded point in each of the graphs below. The synaptic input to the simple from each relay cell is taken to be proportional to the relay cell's spike rate. The scaled sum (mean) of all 9 inputs is shown as the while horizontal line in each graph. (AVI 846 kb)

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Priebe, N., Ferster, D. Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 9, 552–561 (2006). https://doi.org/10.1038/nn1660

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