Spontaneous movements and their relationship to neural activity fluctuate with latent engagement states

Chaoqun Yin; Maxwell D Melin; Gabriel Rojas-Bowe; Xiaonan Richard Sun; João Couto; Steven Gluf; Alex Kostiuk; Simon Musall; Anne K Churchland

doi:10.1016/j.neuron.2025.06.001

Spontaneous movements and their relationship to neural activity fluctuate with latent engagement states

Neuron. 2025 Jun 30:S0896-6273(25)00432-5. doi: 10.1016/j.neuron.2025.06.001. Online ahead of print.

Authors

Chaoqun Yin¹, Maxwell D Melin², Gabriel Rojas-Bowe¹, Xiaonan Richard Sun³, João Couto⁴, Steven Gluf⁵, Alex Kostiuk², Simon Musall⁶, Anne K Churchland⁷

Affiliations

¹ UCLA Neuroscience Interdepartmental Program, Los Angeles, CA 90095, USA; Department of Neurobiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
² UCLA Neuroscience Interdepartmental Program, Los Angeles, CA 90095, USA; Department of Neurobiology, University of California, Los Angeles, Los Angeles, CA 90095, USA; UCLA-Caltech Medical Scientist Training Program, Los Angeles, CA 90095, USA.
³ Section of Neurosurgery, Dartmouth-Hitchcock Medical Center, Lebanon, NH 03756, USA.
⁴ Department of Neurobiology, University of California, Los Angeles, Los Angeles, CA 90095, USA.
⁵ Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
⁶ Institute of Biological Information Processing (IBI-3), Forschungszentrum Jülich, 52428 Jülich, Germany; Department of Systems Neurophysiology, Institute for Zoology, RWTH Aachen University, 52074 Aachen, Germany; Faculty of Medicine, Institute of Experimental Epileptology and Cognition Research, University of Bonn, 53127 Bonn, Germany.
⁷ Department of Neurobiology, University of California, Los Angeles, Los Angeles, CA 90095, USA. Electronic address: achurchland@mednet.ucla.edu.

PMID: 40602403
DOI: 10.1016/j.neuron.2025.06.001

Abstract

Switching between cognitive states is a natural tendency, even for trained experts. To test how cognitive states impact neural activity and behavior, we measured cortex-wide neural activity during decision-making in mice. During disengagement, neural activity was more variable across trials and could be better explained by a linear encoding model. This increase in explained variance during disengagement was associated with two changes: modestly stronger neural encoding of movements generally and an increase in task-independent movements specifically. Surprisingly, behavioral videos showed similar motion energy in both cognitive states. But while the overall amount of movements remained similar, movement alignment changed: as animals slipped into disengagement, their movements became less stereotyped. These idiosyncratic movements were a strong predictor of task performance and engagement. Taken together, our results suggest that the temporal structure of movement patterns constitutes an embodied signature of the cognitive state with a profound relationship to neural activity.

Keywords: behavioral states; cortex; decision-making; imaging; movement; neural encoding model.