Habit learning supported by efficiently controlled network dynamics in naive macaque monkeys

Primates display a marked ability to learn habits in uncertain and dynamic environments. The associated perceptions and actions of such habits engage distributed neural circuits. Yet, precisely how such circuits support the computations necessary for habit learning remain far from understood. Here we construct a formal theory of network energetics to account for how changes in brain state produce changes in sequential behavior. We exercise the theory in the context of multi-unit recordings spanning the caudate nucleus, pre- frontal cortex, and frontal eye fields of female macaque monkeys en- gaged in 60-180 sessions of a free scan task that induces motor habits. The theory relies on the determination of effective connectivity between recording channels, and on the stipulation that a brain state is taken to be the trial-specific firing rate across those channels. The theory then predicts how much energy will be required to transition from one state into another, given the constraint that activity can spread solely through effective connections. Consistent with the theory’s predictions, we observed smaller energy requirements for transitions between more similar and more complex trial saccade patterns, and for sessions characterized by less entropic selection of saccade patterns. Using a virtual lesioning approach, we demonstrate the resilience of the observed relationships between minimum control energy and behavior to significant disruptions in the inferred effective connectivity. Our theoretically principled approach to the study of habit learning paves the way for future efforts examining how behavior arises from changing patterns of activity in distributed neural circuitry.