UCSF

The superior colliculus (SC) is a highly conserved sensorimotor midbrain structure implicated in the control of orienting movements. Yet, despite decades of research, it remains unclear how neural activity in this structure unfolds during internally-driven behaviors like spatial navigation, when orienting movements need to be coordinated with other ongoing behavioral and cognitive processes. This dissertation aims to address this gap. By recording from neurons in the intermediate and deep motor layers of the SC (dSC) of mice navigating a Y-maze, it is demonstrated that: 1) About 30% of neurons fire selectively for left or right turns at the maze bifurcation (left- or right-preferring ‘turn cells’). 2) Turn cell activity is rhythmically modulated during locomotion, firing in-phase with the ongoing stepping cycle of the animal, such that left and right turn cells fire at opposite phases of the stepping cycle. 3) Simultaneous recordings from turn cells and populations of hippocampal place cells reveal that turn cell activity is modulated in directional coordination with hippocampal representations of possible future paths (i.e., hippocampal ‘sweeps’). Critically, hippocampal sweeps prior to the bifurcation can predict turn cell activity at the bifurcation. 4) Consistent with an influence of hippocampal sweeps on turn cell activity, sweeps are associated with biases in the animal’s trajectory toward the represented path. 5) The remaining 70% of neurons in the dSC either exhibit no turn-selective firing at the maze bifurcation or exhibit turn-selective firing that depends on the animal’s starting position on the maze and its upcoming trajectory. Notably, these neurons can exhibit firing that encodes trajectories between two specific maze arms or trajectories converging on a single maze arm.Thus, during navigation, neural activity in the motor layers of the SC reflects not only multiple aspects of ongoing behavior—such as turns, steps, and trajectories—but also ongoing cognitive processes, such as internal representations of possible future paths. These results are consistent with the interpretation that the SC functions as a ‘movement template’, organized as an entire sequence of goal-directed movements, which can be used by higher brain centers for intentional actions (Ewert, 1970; Ingle, 1970; Schaefer, 1970). Drawing on 19th-century psychology, particularly the notion of ‘ideo-motor’ action (Carpenter, 1852; James, 1890), it is further hypothesized the SC plays a central role in transforming cognitive inputs into orienting movements, thereby linking thoughts to actions.