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Electrophysiological signatures of veridical head direction in humans

Abstract

Information about heading direction is critical for navigation as it provides the means to orient ourselves in space. However, given that veridical head-direction signals require physical rotation of the head and most human neuroimaging experiments depend upon fixing the head in position, little is known about how the human brain is tuned to such heading signals. Here we adress this by asking 52 healthy participants undergoing simultaneous electroencephalography and motion tracking recordings (split into two experiments) and 10 patients undergoing simultaneous intracranial electroencephalography and motion tracking recordings to complete a series of orientation tasks in which they made physical head rotations to target positions. We then used a series of forward encoding models and linear mixed-effects models to isolate electrophysiological activity that was specifically tuned to heading direction. We identified a robust posterior central signature that predicts changes in veridical head orientation after regressing out confounds including sensory input and muscular activity. Both source localization and intracranial analysis implicated the medial temporal lobe as the origin of this effect. Subsequent analyses disentangled head-direction signatures from signals relating to head rotation and those reflecting location-specific effects. Lastly, when directly comparing head direction and eye-gaze-related tuning, we found that the brain maintains both codes while actively navigating, with stronger tuning to head direction in the medial temporal lobe. Together, these results reveal a taxonomy of population-level head-direction signals within the human brain that is reminiscent of those reported in the single units of rodents.

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Fig. 1: Experiment outline.
Fig. 2: Electrophysiological activity tracks change in head angle.
Fig. 3: Intracranial electrophysiological activity tracks change in heading angle.
Fig. 4: Electrophysiological activity tracks change in head angle independent of location.
Fig. 5: Electrophysiological representations of location-independent and location-dependent head-direction signals.
Fig. 6: Electrophysiological representations of environment-based head-direction and body-based head-rotation signals.
Fig. 7: Visual depiction of analysis pipeline for experiment 1.

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Data availability

Data acquired from the healthy participants are available at Ludwig-Maximilians-Universität via https://data.ub.uni-muenchen.de/439/ (ref. 87). Due to privacy laws, data acquired from the patients are not openly available, though (subject to privacy laws) can be provided by contacting the corresponding author. Source data are provided with this paper.

Code availability

Openly available at GitHub via https://github.com/benjaminGriffiths/human-hd (ref. 88).

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Acknowledgements

This work was supported by the European Research Council (https://erc.europa.eu/, starting grant 802681 awarded to T. Schreiner) and the Leverhulme Trust (https://www.leverhulme.ac.uk/, early career fellowship ECF-2021-628 awarded to B.J.G.). We thank all participants and in particular all patients who volunteered to participate in this study. We thank the staff and physicians at the Epilepsy Center, Department of Neurology, Ludwig-Maximilians-Universität, Munich, for assistance. We thank A. Chowdhury for valuable input. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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B.J.G.: conceptualization, methodology, software, validation and formal analysis; investigation; data curation; writing—original draft; writing—review and editing; and visualization. T. Schreiner: conceptualization, methodology, investigation, data curation and writing—review and editing. J.K.S.: investigation, data curation and writing—review and editing. C.V.: resources and writing—review and editing. E.K.: resources and writing—review and editing. S.Q.: resources and writing—review and editing. J.R.: resources and writing—review and editing. S.N.: resources and writing—review and editing. T. Staudigl: conceptualization, methodology and investigation; writing—original draft; and writing—review and editing, supervision, project administration and funding acquisition.

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Correspondence to Tobias Staudigl.

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Griffiths, B.J., Schreiner, T., Schaefer, J.K. et al. Electrophysiological signatures of veridical head direction in humans. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01872-1

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