Dynamic Synchronization between Hippocampal Spatial Representations and the Stepping Rhythm

Abstract

Summary paragraphThe hippocampus is a vertebrate brain structure that expresses spatial representations1 and is critical for navigation2,3. Navigation in turn intricately depends on locomotion; however, current accounts suggest a dissociation between hippocampal spatial representations and the details of locomotor processes. Specifically, the hippocampus is thought to primarily represent higher-order cognitive and locomotor variables like position, speed, and direction of movement4–7, while the limb movements that propel the animal are thought to be computed and represented primarily in subcortical circuits, including the spinal cord, brainstem, and cerebellum8–11. Whether hippocampal representations are actually decoupled from the detailed structure of locomotor processes remains unknown. To address this question, we simultaneously monitored hippocampal spatial representations and ongoing limb movements underlying locomotion at fast timescales. We found that the forelimb stepping cycle in freely behaving rats is rhythmic and peaks at ~8 Hz during movement, matching the ~8 Hz organization of information processing in the hippocampus during locomotion12. We also discovered precisely timed coordination between the time at which the forelimbs touch the ground (‘plant’ times of the stepping cycle) and the hippocampal representation of space. Notably, plant times coincide with hippocampal representations closest to the actual position of the animal, while in-between these plant times, the hippocampal representation progresses towards possible future locations. This synchronization was specifically detectable when animals approached upcoming spatial decisions. Taken together, our results reveal profound and dynamic coordination on a timescale of tens of milliseconds between central cognitive representations and peripheral motor processes. This coordination engages and disengages rapidly in association with cognitive demands and is well suited to support rapid information exchange between cognitive and sensory-motor circuits.