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This article will pose the following challenge: that despite four decades of research characterizing the response properties of V1 neurons, we still do not have a decent picture of how V1 really operates---i.e., how a population of its neurons represents natural scenes under realistic viewing conditions. We identify five problems with the current view that stem largely from biases in the design and execution of experiments, in addition to the contributions of non-linearities in the cortex that are not well understood. Our purpose is to open the window to new theories, a number of which we describe along with some proposals for testing them.

In the visual cortex of the cat and ferret, it is established that maturation of orientation selectivity is shaped by experiencedependent plasticity. However, recent experiments indicate that orientation maps are remarkably stable and experienceindependent. We present a model to account for these seemingly paradoxical results. In this model, a scaffold consisting of non-isotropic lateral connections is laid down in horizontal circuitry before visual experience. These lateral connections provide an experience-independent framework for the developing orientation maps by inducing a broad orientation tuning bias in the model neurons. Experience-dependent plasticity of the thalamocortical connections sharpens the tuning while the preferred orientation of the neurons remains unchanged. This Rearing experiments have established that synaptic connections in the geniculocortical pathway are highly plastic during early

We review theoretical and experimental results on the processing of layer 4, the input-recipient layer, of cat primary visual cortex (V1). A wide range of experimental data can be understood from a model in which response tuning of layer 4 cells is largely determined by a local interplay of feedforward excitation (from thalamus) and feedforward inhibition (from layer 4 inhibitory interneurons driven by thalamus). Feedforward inhibition dominates excitation, inherits its tuning from the thalamic input, and sharpens the tuning of excitatory cells. At least a strong component of the feedforward inhibition received by a cell is spatially opponent to the excitation it receives, meaning that inhibition is driven by dark in regions of the visual field in which excitation is driven by light, and vice versa. The idea of opponent inhibition can be generalized to mean inhibition driven by input patterns that are strongly anticorrelated with the patterns that excite a cell. We argue that dominant feedforward opponent inhibition may be a general principle of cortical layer 4. This leads to the suggestion that the properties that show columnar organization -- invariance across the vertical depth of cortex -- may be properties that are shared by "opposite" (anticorrelated) stimulus pairs. This contrasts with the more common idea that a column represents a set of cells that all share similar stimulus preferences.

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In what regime does the cortical circuit operate? Our intracellular studies of surround suppression in cat primary visual cortex (V1) provide strong evidence on this question. Although suppression has been thought to arise from an increase in lateral inhibition, we find that the inhibition that cells receive is reduced, not increased, by a surround stimulus. Instead, suppression is mediated by a withdrawal of excitation. Thalamic recordings and previous work show that these effects cannot be explained by a withdrawal of thalamic input. We find in theoretical work that this behavior can only arise if V1 operates as an inhibition-stabilized network (ISN), in which excitatory recurrence alone is strong enough to destabilize visual responses but feedback inhibition maintains stability. We confirm two strong tests of this scenario experimentally and show through simulation that observed cell-to-cell variability in surround effects, from facilitation to suppression, can arise naturally from variability in the ISN.

In cortical simple cells of cat striate cortex, the response to a visual stimulus of the preferred orientation is partially suppressed by simultaneous presentation of a stimulus at the orthogonal orientation, an eect known as \cross-orientation inhibition". It has been argued that this is due to the presence of inhibitory connections between cells tuned for dierent orientations, but intracellular studies suggest that simple cells receive inhibitory input primarily from cells with similar orientation tuning. Furthermore, response suppression can be elicited by a variety of non-preferred stimuli at all orientations. Here we study a model circuit that was presented previously to address many aspects of simple cell orientation tuning, which is based on local intracortical connectivity between cells of similar orientation tuning. We show that this model circuit can account for many aspects of cross-orientation inhibition and, more generally, of response suppression by non-preferred stimuli and of other non-linear properties of responses to stimulation with multiple gratings.