Coherent dynamics of thalamic head-direction neurons irrespective of input

The generation of the head-direction (HD) signal, a cornerstone of the brain’s 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.