Nonlinear Lateral Interactions in V1 Population Responses Explained by a Contrast Gain Control Model

• Published in: The Journal of neuroscience Vol. 38; no. 47; pp. 10069 - 10079
• Main Authors: Michel, Melchi M, Chen, Yuzhi, Seidemann, Eyal, Geisler, Wilson S
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 21.11.2018
• Subjects: Electrophysiology; Image contrast; Membrane potential; Neuroimaging; Nonlinear control; Nonlinear systems; Nonlinearity; Orientation; Population; Psychophysics; Representations; Spiking; Visual cortex; striate cortex; contrast gain control; voltage-sensitive dye imaging; visual cortex; lateral interactions; population coding
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.0246-18.2018

How do cortical responses to local image elements combine to form a spatial pattern of population activity in primate V1? Here, we used voltage-sensitive dye imaging, which measures summed membrane potential activity, to examine the rules that govern lateral interactions between the representations of two small local-oriented elements in macaque ( ) V1. We find strong subadditive and mostly orientation-independent interactions for nearby elements [2-4 mm interelement cortical distance (IED)] that gradually become linear at larger separations (>6 mm IED). These results are consistent with a population gain control model describing nonlinear V1 population responses to single oriented elements. However, because of the membrane potential-to-spiking accelerating nonlinearity, the model predicts supra-additive lateral interactions of spiking responses for intermediate separations at a range of locations between the two elements, consistent with some prior facilitatory effects observed in electrophysiology and psychophysics. Overall, our results suggest that population-level lateral interactions in V1 are primarily explained by a simple orientation-independent contrast gain control mechanism. Interactions between representations of simple visual elements such as oriented edges in primary visual cortex (V1) are thought to contribute to our ability to easily integrate contours and segment surfaces, but the mechanisms that govern these interactions are primarily unknown. Our study provides novel evidence that lateral interactions at the population level are governed by a simple contrast gain-control mechanism, and we show how this divisive gain-control mechanism can give rise to apparently facilitatory spiking responses.