Alerting acoustic stimuli enhance the internal representation of head direction.

Abstract

Animals rapidly execute goal-directed spatial behaviors in response to threats, yet how alerting cues engage spatial representations remains unknown. Here, we tested whether head direction (HD) neurons-key components of the brain's navigation system-are recruited by alerting stimuli. We recorded thalamic and cortical HD cells in head-fixed mice during alerting acoustic stimuli while monitoring arousal via pupillometry and facial motion. Identified HD cells in the anterodorsal thalamic nucleus exhibited ectopic axons and projections to the thalamic reticular nucleus. These cells responded to artificial and natural alerting sounds, with frequency tuning closely matching facial motion patterns. Thalamic responses comprised fast and slow components, whereas cortical responses in the dorsal presubiculum were sparser and dominated by the slow component. In the thalamus, the fast component was independent of HD tuning, whereas the slow component was selectively amplified by alerting stimuli. This gain modulation enhanced HD coding, with decoding accuracy scaling with facial motion. Together, these findings identify the thalamocortical HD system as a non-canonical auditory pathway relaying alerting signals to spatial navigation circuits, providing a mechanism by which alerting stimuli sharpen the internal compass for goal-directed behaviors.