The head-direction signal is generated by multiple attractor-like networks

Abstract

The generation of the head-direction (HD) signal, a cornerstone of the brains navigation system, is classically attributed to the lateral mammillary nucleus (LMN) and associated brainstem structures, where attractor-like dynamics are thought to maintain population coherence. Here, using multi-site recordings and optogenetic perturbations along the mammillary-thalamic-cortical pathway, we demonstrate that HD neurons in the anterodorsal nucleus of the thalamus (ADN) maintain coherent population dynamics even when their LMN inputs become decorrelated during non-REM sleep. These findings reveal that thalamic coherence does not strictly depend on structured input from the LMN; instead, it can emerge from local thalamic processes involving shared inhibition and non-linear responses. Together, our findings reveal a previously unrecognized, state-dependent shift in the circuit organizing the HD signal, establishing the thalamus as an active substrate capable of independently sustaining internal representations across brain states.