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Synaptic excitation and inhibition in simple cells of primary visual cortex: challenging a classical model of receptive field structure
M. Morgan Taylor, Madineh Sedigh-Sarvestani, Leif E. Vigeland, Larry A. Palmer, and Diego Contreras
University of Pennsylvania

Visual inputs reach the primary visual cortex (V1) in layer 4 (L4) and synapse onto simple cells, where a critical transformation takes place: the center-surround receptive fields (RFs) of thalamic inputs are converted into the elongated RFs of simple cells, with sub-regions of opposing contrasts lying side by side [1]. This structure arises from the spatial arrangement of the excitatory thalamic inputs and a presumed but unknown influence from the engagement of local cortical inhibition. The synaptic structure that underlies the RF is responsible for the visual response properties and input integration of simple cells. Extracellular observations led to a push-pull model of RF organization: within each sub-region, one stimulus contrast increases firing rate (push), while the opposite contrast decreases firing rate (pull) [2]. The mechanisms of push and pull were later interpreted as pure excitatory and inhibitory synaptic processes, respectively [3,4,5]. A synaptic push-pull theory in simple cells would entail opponent excitation and inhibition in response to opposite contrasts within a sub-region, leading to spatially segregated excitation and inhibition across the sub-regions of the RF.

Here, using intracellular recordings in anesthetized cats in vivo from simple, regular spiking cells in V1 (Area 17) L4, we estimate the underlying synaptic structure of their RFs. We use single or pairs of optimally oriented bars flashed at varying time delays and in different positions within the RF, while varying the membrane potential with different levels of current injection. We then calculate synaptic conductance and reversal potential, from which we estimate excitatory and inhibitory conductances.

Our results depart from key predictions of push-pull in at least two ways. First, we find that a stimulus that evokes an excitatory conductance also evokes a comparable inhibitory conductance. We find that this inhibition from excitatory stimuli is delayed relative to excitation. Second, while excitation is spatially segregated according to RF sub-region, we observe broad inhibition across the RF.

We further show that delayed inhibition plays a functional role in reducing the "window of opportunity" [6] for synaptic inputs to trigger spikes. This effectively increases the precision of the cell's output, as we have proposed previously [7], and as we and others have demonstrated in other sensory systems [8,9,10]. Our results show that synaptic inhibition suppresses responses to non-preferred stimuli and thereby shapes the cell's RF. Furthermore, we show that excitatory drive from a preferred stimulus evokes inhibition that dynamically shapes the timing of a V1 simple cell's spiking output, contradicting a synaptic push-pull model.

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