Habit learning is associated with efficiently controlled network dynamics in naive macaque monkeys

Abstract: Primates utilize distributed neural circuits to learn habits in uncertain environments, but the underlying mechanisms remain poorly understood. We propose a formal theory of network energetics explaining how brain states influence sequential behavior. We test our theory on multi-unit recordings from the caudate nucleus and cortical regions of macaques performing a motor habit task. The theory predicts the energy required to transition between brain states represented by trial-specific firing rates across channels, assuming activity spreads through effective connections. We hypothesized that habit formation would correlate with lower control energy. Consistent with this, we observed smaller energy requirements for transitions between similar saccade patterns and those of intermediate complexity, and sessions exploiting fewer patterns. Simulations ruled out confounds from neurons' directional tuning. Finally, virtual lesioning demonstrated robustness of observed relationships between control energy and behavior. This work paves the way for examining how behavior arises from changing activity in distributed circuitry.