Neural correlates of perceptual decision making in primary somatosensory cortex

The brain is thought to produce decisions by gradual accumulation of sensory evidence ¹ through a hierarchically organized feedforward cascade of neuronal activities that transforms early stimulus representations in the primary somatosensory cortex (S1) ² to a perceptual decision processed in pre-motor areas ^3–6 . Recently, this prevailing view has been challenged by observation of choice-correlated neural activity as early in the hierarchy as S1 ^7–13 . Here, to reconcile these seemingly controversial observations, we employ ethological whisker-guided navigation of mice in a tactile virtual reality paradigm ^14–16 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 ¹⁶ . We show that neural activity in principal whisker wS1 barrel recorded during untrained and unrewarded two alternative forced choice (2AFC) decision-making consists of “fast” (50ms) and “slow” (200-300ms) stages that are mostly orthogonal to each other and directly precede the decision execution. The fast component represents detection of a deviant signal in sensory perception, that triggers 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 ^1,5,17,18 . 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 ^17,18 to be transformed into perception and action.