Population dynamics of choice representation in dorsal premotor and primary motor cortex

Studies in multiple species have revealed the existence of neural signals that lawfully co-vary with different aspects of the decision-making process, including choice, sensory evidence that supports the choice, and reaction time. These signals, often interpreted as the representation of a decision variable (DV), have been identified in several motor preparation circuits and provide insight about mechanisms underlying the decision-making process. However, single-trial dynamics of this process or its representation at the neural population level remain poorly understood. Here, we examine the representation of the DV in simultaneously recorded neural populations of dorsal premotor (PMd) and primary motor (M1) cortices of monkeys performing a random dots direction discrimination task with arm movements as the behavioral report. We show that single-trial DVs covary with stimulus difficulty in both areas but are stronger and appear earlier in PMd compared to M1 when the stimulus duration is fixed and predictable. When temporal uncertainty is introduced by making the stimulus duration variable, single-trial DV dynamics are accelerated across the board and the two areas become largely indistinguishable throughout the entire trial. These effects are not trivially explained by the faster emergence of motor kinematic signals in PMd and M1. All key aspects of the data were replicated by a computational model that relies on progressive recruitment of units with stable choice-related modulation of neural population activity. In contrast with several recent results in rodents, decision signals in PMd and M1 are not carried by short sequences of activity in non-overlapping groups of neurons but are instead distributed across many neurons, which once recruited, represent the decision stably during individual behavioral epochs of the trial.