Non-canonical attractor dynamics underlie perceptual decision-making

Abstract

Perceptual decision-making is the process by which an animal uses sensory stimuli to choose an action or mental proposition. This process is thought to be mediated by neurons organized as attractor networks1,2. However, whether attractor dynamics underlie decision behavior and the complex neuronal responses remains unclear. Here we use simultaneous recordings from hundreds of neurons, together with an unsupervised, deep learning-based method, to discover decision-related neural dynamics in frontal cortex and striatum of rats while the subjects accumulate pulsatile auditory evidence. We found that trajectories evolved along two sequential regimes, the first dominated by sensory inputs, and the second dominated by the autonomous dynamics, with flow in a direction (i.e., "neural mode") largely orthogonal to that in the first regime. We propose that the transition to the second regime corresponds to the moment of decision commitment. We developed a simplified model that approximates the coupled transition in dynamics and neural mode and allows precise inference, from each trials large-scale neural population activity, of a putative neurally-inferred time of commitment ("nTc") on that trial. The simplified model captures diverse and complex single-neuron temporal profiles, such as ramping and stepping3-5, as well as trial-averaged curved trajectories6-8, and reveals distinctions between brain regions. The estimated nTc times were not time-locked to stimulus onset or offset, or to response onset, but were instead broadly distributed across trials. If nTc marks the moment of decision commitment, sensory evidence before nTc should affect the decision, while evidence afterward should not. Behavioral analysis of trials aligned to their estimated nTc times confirmed this prediction. Our results show that the formation of a perceptual choice involves a rapid, coordinated transition in both the dynamical regime and the neural mode of the decision process that corresponds to commitment to a decision, and suggest this moment as a useful entry point for dissecting mechanisms underlying rapid changes in internal state.