Functional coupling between target selection and acquisition in the superior colliculus.

Abstract

Survival in unpredictable environments requires that animals continuously evaluate their surroundings for behavioral targets, direct their movements toward those targets, and terminate movements once a target is reached. The ability to select, move toward, and acquire spatial targets depends on a network of brain regions, but it remains unknown how these goal-directed processes are linked by neural circuits. Within this network, common circuits in the midbrain superior colliculus (SC) mediate the selection and initiation of movements to spatial targets. However, SC activity often persists throughout movement, suggesting that the same SC circuits underlying target selection and movement initiation may also contribute to "target acquisition": stopping the movement at the selected target. Here, we examine the hypothesis that SC functional circuitry couples target selection and acquisition using a "default motor plan" generated by selection-related neuronal activity. Recordings from intermediate and deep layer SC neurons in mice performing a spatial choice task demonstrate that choice-predictive neurons, including optogenetically identified GABAergic neurons whose activity mediates target selection, exhibit increased activity during movement to the target. By recording from rostral and caudal SC in separate groups of mice, we also revealed higher activity in rostral than caudal neurons during target acquisition. Finally, we used an attractor model to examine how-invoking only SC circuitry-caudal SC activity related to selecting an eccentric target could generate higher rostral than caudal acquisition-related activity. Overall, our results suggest a functional coupling between SC circuits for target selection and acquisition, elucidating a key mechanism for goal-directed behavior.NEW & NOTEWORTHY How do neural circuits ensure that selected targets are successfully acquired? Here, we examine whether choice-related activity in the superior colliculus (SC) promotes a motor plan for target acquisition. By demonstrating that choice-predictive SC neurons-including GABAergic neurons-remain active throughout movement, while the activity of rostral SC neurons increases during acquisition, and by recapitulating these dynamics with an attractor model, our results support a role for SC circuits in coupling target selection and acquisition.