Distinct neural signatures of hippocampal population dynamics during locomotion-in-place

Hippocampal CA1 neurons modulate their activity with movement variables such as time, distance, and speed, yet it remains unclear how these representations reorganize across behavioral states, from externally driven to self-paced movement and immobility. Here, we investigated how sensory events that initiate or terminate locomotion, structure CA1 population codes and how these codes reorganize across sensory-driven locomotion, spontaneous locomotion, and forced immobility. Using two-photon calcium imaging in head-fixed Thy1-GCaMP mice (n = 5) performing the air-induced running task on a non-motorized conveyor belt, we examined neuronal firing-rate modulation across a series of behavioral configurations designed to probe distinct forms of locomotion-in-place. In the No-Brake (locomotion-permitted) condition, the belt rotated freely, allowing animals to execute full cyclic limb movements in response to air stimulation. In the Brake (immobility) condition, the belt was fixed, restricting movement to partial or attempted locomotor motions. Firing-rate modulation with respect to time, distance, and speed was quantified using linear (Pearson correlation) and nonlinear (mutual information) metrics under permutation testing in the natural reference domains. Behaviorally, air stimuli produced faster, sustained running during air-on and more variable, self-paced movement during air-off. Neurally, a larger fraction of CA1 cells was active and significantly modulated during air-off attributed to its longer duration. Within the modulated set, singularly tuned cells (time, distance, or speed) predominated over mixed-tuned cells, and speed-modulated cells peaked earlier after stimulus onset or offset than time- or distance-modulated cells suggesting temporal precedence. Under Brake, CA1 activity was predominantly singularly tuned to time or movement-in-place, with stronger movement modulation and engagement post-stimulation. Despite substantial single-cell turnover across configurations and phases, population-level analyses revealed a coherent, air-phase-locked organization and distinct movement-related populations across Brake and No-Brake conditions. These results indicate a state-dependent reweighting of sensorimotor features implemented atop a conserved ensemble scaffold in CA1.