Vestibular compound action potentials and macular velocity evoked by sound and vibration in the guinea pig

To examine mechanisms responsible for vestibular afferent sensitivity to transient air conducted sounds (ACS) and inter-aural bone conducted vibration (BCV), we performed simultaneous measurements of stimulus-evoked vestibular compound action potentials (vCAPs), utricular macula or stapes velocity, and Vestibular Microphonics (VMs) in the anaesthetized guinea pig. For short duration punctate stimuli (<1ms), the vCAP increases magnitude in close proportion to macular velocity and temporal bone (ear-bar) acceleration, rather than other kinematic variables. For longer duration stimuli, the vCAP magnitude switches from acceleration sensitive to linear jerk sensitive. vCAP input-output (IO) functions suggest primary afferent response generation has the same origins for both BCV and ACS, with similar macular velocity thresholds and IO functions for both stimuli. Frequency tuning curves evoked by tone-burst stimuli also show the vCAP increases magnitude in proportion to macular velocity, while in contrast, the VM increases magnitude in proportion to macular displacement across the entire frequency bandwidth tested. The subset of vestibular afferent neurons responsible for synchronized firing and vCAPs make calyceal synaptic contacts with type I hair cells in the striolar region of the epithelium and have irregularly spaced inter-spike intervals at rest. Present results provide new insight into mechanical and neural mechanisms underlying synchronized action potentials in these sensitive afferents, with clinical relevance for understanding the activation and tuning of neurons responsible for driving rapid compensatory reflex responses.