An anatomically constrained model of V1 simple cells predicts the coexistence of push-pull and broad inhibition

Jan Antolik, Morgan Taylor, Diego Contreras, Alain Destexhe and Yves Frégnac

Journal of Neuroscience (in press, 2021)

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The spatial organization and dynamic interactions between excitatory and inhibitory synaptic inputs that define the receptive field (RF) of simple cells in cat primary visual cortex (V1) still raise paradoxical issues: 1) stimulation of simple cells in V1 with drifting gratings supports a wiring schema of spatially segregated sets of excitatory and inhibitory inputs activated in an opponent way by stimulus contrast polarity; 2) in contrast, intracellular studies using flashed bars suggest that, while ON and OFF excitatory input are indeed segregated, inhibitory inputs span the entire RF irrespective of input contrast polarity. Here, we propose a biologically detailed computational model of simple cells embedded in a V1-like network that resolves this seeming contradiction. We varied parametrically the RF-correlation-based bias for excitatory and inhibitory synapses and found that a moderate bias of excitatory neurons to synapse onto other neurons with correlated receptive fields, and a weaker bias of inhibitory neurons to synapse onto other neurons with anti-correlated receptive fields can explain the conductance input, the postsynaptic membrane potential, and the spike train dynamics under both stimulation paradigms. This computational study shows that the same structural model can reproduce the functional diversity of visual processing observed during different visual contexts.
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