Hippocampal theta aligns to paw movements during a forelimb-dominated sensorimotor behavior

Hippocampal theta oscillations organize the timing of neural activity to support navigation, memory formation, and sensorimotor integration. Theta is modulated by running speed, breathing, whisking, and jumping. For example, the positive relationship between theta frequency and running speed is believed to stabilize hippocampal representations of space amid movement variability. Furthermore, alignment between theta phase and single-unit activity to task-relevant movements suggests a role for theta in sensorimotor integration. While associations between theta and locomotion have been studied extensively, less is known about relationships between theta and movement during non-locomotor tasks. Here, hippocampal theta was examined during a novel string-pulling task to determine if established relationships between theta frequency, power, and phase locking to movement extend to skilled reaching and grasping behaviors. In this task, vestibular, hindlimb, and visual flow signals are limited, but animals still traverse a “space” (length of string) to acquire a reward. Five Sprague Dawley rats (4 mo.) were trained to perform a novel string-pulling task where reward was delivered only after a predefined length of string was pulled. Behavior was measured using high-speed video recording and DeepLabCut, allowing considerable precision in the analysis of individual paw movements and the categorization of each movement into lift, advance, grasp, pull, and push phases. Local field potentials were recorded from electrodes in dorsal CA1. Analysis revealed that the established positive relationship between theta frequency and movement speed reported during running was absent or reversed during string pulling. Theta power and frequency also peaked during the contralateral paw’s downward push, despite paw speed being low during this action. Finally, theta phase became aligned to the pull but not to other movement in the reach-pull cycle. Since phase locking is associated with sensorimotor gating, phase alignment during the pull could reflect the gating of inputs that are most relevant for reaching the reward, potentially facilitating integration of action-outcome information.