Dynamics of thalamic directional coding under vestibular imbalance

Abstract

Head direction cells (HDCs) encode the animals orientation in space and form a core component of the brains navigation system. While their dependence on vestibular input is well established, how directional circuits respond to unilateral vestibular loss (UVL) -- the most frequent and ecologically relevant form of vestibular imbalance -- remains largely unknown. UVL offers a powerful model to investigate how spatial circuits adapt to asymmetric sensory disruption and partial deafferentation. To explore this, we examined the impact of UVL on anterior thalamic nuclei (ATN) activity and spatially tuned neurons in freely moving rats following unilateral vestibular neurectomy (UVN). UVN induced long-lasting alterations in ATN firing dynamics, including reduced theta modulation, diminished burst firing, and selective disruption across functionally defined neuronal classes: head-direction and speed-modulated cells were strongly affected, while angular head velocity and position cells remained largely preserved. Despite initial degradation, HDCs persisted and progressively regained directional tuning. Crucially, spike waveform analysis revealed two distinct HDC subtypes with markedly different vulnerabilities: one subtype showed reduced prevalence and degraded tuning, whereas the other remained resilient and supported the recovery of directional coding. These findings uncover a previously unrecognized heterogeneity within the head direction system and show that compensation following UVL is partial, cell type-specific, and functionally selective. Together, they offer new insight into sensory plasticity within thalamic navigation circuits and provide a framework to understand spatial deficits associated with vestibular imbalance.