Tiltable objective microscope visualizes discrimination of static and dynamic head movement originates at hair cells

Abstract Spatio-temporal information on head orientation and movement is fundamental to the sense of balance and motion. Hair cells (HCs) in otolith organs of the vestibular system transduce linear acceleration, including head tilt and vibration. Here, we build a tiltable objective microscope in which an objective lens and specimen tilt together. In vivo Ca2+ imaging of all utricular HCs and ganglion neurons during 360° static tilt and vibration in pitch and roll axes visualizes the direction- and modality-selective topographic responses in larval zebrafish. We find that head vibration is preferentially received by HCs in a specific region whereas static tilt is preferentially transduced by HCs in the outside region. Spatially ordered direction preference in HCs is consistent with hair-bundle polarity, and is preserved in ganglion neurons through topographic innervation. Together, these results demonstrate that the discrimination of different direction and temporal modalities of head orientation and movement originates at HCs.