An Anatomically Constrained Model of V1 Simple Cells Predicts the Coexistence of Push–Pull and Broad Inhibition
Résumé
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.Significance StatementIdentifying generic connectivity motives in cortical circuitry encoding for specific functions is crucial for understanding the computations implemented in cortex. Indirect evidence points to correlation-based biases in connectivity pattern in V1 of higher mammals, whereby excitatory and inhibitory neurons preferentially synapse onto neurons respectively with correlated and anti-correlated receptive fields. A recent intracellular study questions this "push-pull" hypothesis, failing to find spatial anti-correlation patterns between excitation and inhibition across the receptive field. We present here a spiking model of V1 that integrates relevant anatomical and physiological constraints, and shows that a more versatile motif of correlation-based connectivity with selectively tuned excitation and broadened inhibition is sufficient to account for the diversity of functional descriptions obtained for different classes of stimuli.
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