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Peer-reviewedCC BY 4.0Nature Communications

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

Abstract

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.

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BibTeX
@article{pak2026active,
  title = {{Active locomotion predictively rescues head direction attractor dynamics in head-fixed mice}},
  author = {Alexandr Pak and Janna Aarse and Heng Wei Zhu and Jean-Paul Noel and Simón Carrillo Segura and André A. Fenton and Dora Angelaki},
  journal = {Nature Communications},
  year = {2026},
  month = oct,
  doi = {10.1038/s41467-026-79031-5},
  url = {https://www.nature.com/articles/s41467-026-79031-5},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Active locomotion predictively rescues head direction attractor dynamics in head-fixed mice
AU  - Alexandr Pak
AU  - Janna Aarse
AU  - Heng Wei Zhu
AU  - Jean-Paul Noel
AU  - Simón Carrillo Segura
AU  - André A. Fenton
AU  - Dora Angelaki
PY  - 2026
DA  - 2026/10/25
JO  - Nature Communications
DO  - 10.1038/s41467-026-79031-5
UR  - https://www.nature.com/articles/s41467-026-79031-5
AB  - 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.
SN  - 2041-1723
ER  -