Neural correlates of perceptual decision making in primary somatosensory cortex

Abstract

The brain is thought to produce decisions by gradual accumulation of sensory evidence through a hierarchically organized feedforward cascade of neuronal activities that transforms early stimulus representations in the primary somatosensory cortex (S1) to a perceptual decision processed in pre-motor areas. Recently, this prevailing view has been challenged by observation of choice- correlated neural activity as early in the hierarchy as S1. Here, to reconcile these seemingly controversial observations, we employ ethological whisker-guided navigation of mice in a tactile virtual reality paradigm combined with dense electrophysiological recordings in whisker-related wS1. Leaving only a pair of C2 whiskers for mice to navigate with, we effectively designed an information bottleneck for sensory input to decision making. We show that neural activity during sensory evidence accumulation exhibits dramatic collapse of the high-dimensional spiking activity to just a single latent variable followed by a slower and almost synchronous ramping up across the whole cortical column. We show that this variable is consistent with models of gradual accumulation of noisy sensory evidence to a decision bound. These observations indicate that S1 may directly participate in a categorical coding of all-or-none decision variable via cortico-cortical feedback loops through which sensory information reverberates to be transformed into perception and action. Significance StatementBy employing ethological whisker-guided navigation of mice in a tactile virtual reality paradigm combined with dense electrophysiological recordings in whisker-related wS1, we show that neural activity during sensory evidence accumulation exhibits dramatic collapse of the high-dimensional spiking activity to just a single latent variable followed by a slower and almost synchronous ramping up across the whole cortical column. We show that this variable is consistent with models of gradual accumulation of noisy sensory evidence to a decision bound. These observations indicate that wS1 may directly participate in a categorical coding of all-or-none decision variable. Naturalistic perceptual decisions during active whisker-guided navigation High-dimensional activity in S1 collapses to a single variable prior to decision This ramping spiking activity is consistent with drift-diffusion decision models Indicates direct involvement of S1 in evidence accumulation