Metastable attractors explain the variable timing of stable behavioral action sequences

Abstract

The timing of self-initiated actions shows large variability even when they are executed in stable, well-learned sequences. Could this mix of reliability and stochasticity arise within the same neural circuit? We trained rats to perform a stereotyped sequence of self-initiated actions and recorded neural ensemble activity in secondary motor cortex (M2), which is known to reflect trial-by-trial action-timing fluctuations. Using hidden Markov models, we established a dictionary between activity patterns and actions. We then showed that metastable attractors, representing activity patterns with a reliable sequential structure and large transition timing variability, could be produced by reciprocally coupling a high-dimensional recurrent network and a low-dimensional feedforward one. Transitions between attractors relied on correlated variability in this mesoscale feedback loop, predicting a specific structure of low-dimensional correlations that were empirically verified in M2 recordings. Our results suggest a novel mesoscale network motif based on correlated variability supporting naturalistic animal behavior.