Conjoint specification of action by neocortex and striatum

Neuron. 2025 Jan 16:S0896-6273(24)00922-X. doi: 10.1016/j.neuron.2024.12.024. Online ahead of print.

Abstract

The interplay between two major forebrain structures-cortex and subcortical striatum-is critical for flexible, goal-directed action. Traditionally, it has been proposed that striatum is critical for selecting what type of action is initiated, while the primary motor cortex is involved in specifying the continuous parameters of an upcoming/ongoing movement. Recent data indicate that striatum may also be involved in specification. These alternatives have been difficult to reconcile because comparing very distinct actions, as is often done, makes essentially indistinguishable predictions. Here, we develop quantitative models to reveal a somewhat paradoxical insight: only comparing neural activity across similar actions makes strongly distinguishing predictions. We thus developed a novel reach-to-pull task in which mice reliably selected between two similar but distinct reach targets and pull forces. Simultaneous cortical and subcortical recordings were uniquely consistent with a model in which cortex and striatum jointly specify continuous parameters governing movement execution.

Keywords: action selection; action specification; basal ganglia; computational model; motor control; motor cortex; neuropixels; optogenetics; reinforcement learning; striatum.