Environment-specific virtual head direction representation in the human anteroventral thalamus during memory-guided...

Knowing which way you are facing is essential for navigation. In animals, a dedicated set of neurons-head direction cells-acts as an internal compass: each cell fires most strongly when the animal faces a particular direction. The anterior thalamus is a key hub for this system. In humans, however, direct electrophysiological evidence for a comparable head direction signal remains limited. To address this gap, we recorded intracranial electroencephalography (EEG) from the anteroventral thalamus (AVT) in patients with epilepsy while they performed a virtual navigation task. We analyzed neural activity during in-place rotation to isolate virtual head direction (vHD) information. Using inverted encoding models applied to multi-band neural activity, we reconstructed continuous vHD within two distinct virtual environments. Critically, the decoders failed to generalize across environments, indicating that the AVT vHD representation is environment specific rather than a fixed, universal map. This encoding was observed in the AVT and was temporally specific to rotation epochs; no significant encoding was detected in the pulvinar, another thalamic subregion not part of the classic head direction network in rodents. Together, these findings suggest that the human AVT carries environment-specific vHD information, bridging a gap between animal models and human navigation and highlighting a potential link to spatial disorientation disorders.