Active locomotion predictively rescues head direction attractor dynamics in head-fixed mice

Head direction (HD) cells in the anterodorsal thalamic nucleus form the brain’s internal compass, and are often modeled as a ring attractor maintaining azimuth coding by leveraging continuous visual and inertial sensory input. Here, we test how the common experimental preparation of head-fixed animals alters this code. Complete head-fixation that creates vestibular conflict disrupts both unit and population encoding of head direction, while selectively constraining head-on-body movements either in real or virtual reality uniquely impairs HD population activity.

More specifically, attractor dynamics are altered in head-restrained male mice during periods of immobility, and a computational model recapitulates this effect by perturbing lateral connectivity among HD neurons. These dynamics recover several hundred milliseconds prior to locomotion onset, suggesting that an efference copy or prediction of a re-afferent signal is necessary to maintain HD network activity during head restraint. More generally, the results indicate that the HD network is a context- and state-dependent predictive estimator, stabilized by forthcoming self-motion signals.

The classic ring-attractor models should be revised to integrate context-dependent dynamics with prospective motor signals, offering a more complete account of how the brain’s compass remains stable across both naturalistic and constrained conditions. We thank Angelaki and Fenton lab members for their insightful discussions. This work has been funded by NIH DC004260, Simons Collaboration for the Global Brain (SCGB) SFI-AN-NC-GB-Culmination-00002796.

A.P. was supported by Nazarbayev University under Faculty-development competitive research grants program for 2025-2027 (Grant No. 040225FD4718). J.N. was additionally supported by NIH NINDS R00NS128075, the Simons Collaboration in Ecological Neuroscience (SFI-AN-NC-SCN-00007276-10 and SFI-AN-AR-Pilot-00008952), CTSI 1UM1TR004405, and a Sloan Research Fellowship. These authors contributed equally: Alexandr Pak, Janna Aarse.

Department of Biological and Biomedical Sciences, School of Medicine, Nazarbayev University, Kabanbay batyr 53, Astana, 010000, Kazakhstan Department of Neurophysiology, Ruhr University Bochum, Bochum, Germany Center for Neural Science, New York University, New York, NY, 10003, USA Janna Aarse, Heng Wei Zhu, Simón Carrillo Segura, André A. Fenton & Dora Angelaki Department of Neuroscience, University of Minnesota, Minneapolis, MN, 55455, USA The authors declare no competing interests. Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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