A canonical input to the head direction compass carries predominantly eye movement signals

Abstract

The mammalian head direction (HD) system is thought to update its internal compass using angular head velocity (AHV) signals relayed from the brainstem. We tested this canonical interpretation by recording from the nucleus prepositus hypoglossi (NPH), a proposed AHV relay known to be important for accurate HD tracking, while simultaneously measuring eye and head movements in mice. Neurons classified as AHV-tuned instead predominantly encoded eye movements: most showed saccade-related bursts or pauses, and apparent AHV tuning was largely explained by eye rather than head motion. Optotagging showed that even NPH neurons projecting directly to the HD circuit predominantly encoded eye movements. Empirically constrained population models reconstructed eye position and gaze direction, but head-direction readouts failed when eye and head motion were dissociated. These findings overturn the canonical view of NPH as a dedicated AHV relay, revealing eye movements as a major, previously unmeasured component of the signals entering the mammalian HD circuit and thereby changing the computational problem that the HD system must solve to maintain a stable representation of heading.