Prior Acoustic Trauma Alters Type II Afferent Activity in the Mouse Cochlea

Auditory stimuli travel from the cochlea to the brainstem through type I and type II cochlear afferents. While type I afferents convey information about the frequency, intensity, and timing of sounds, the role of type II afferents remains unresolved. Limited recordings of type II afferents from cochlear apex of prehearing rats reveal they are activated by widespread outer hair cell stimulation, ATP, and by the rupture of nearby outer hair cells. Altogether, these lines of evidence suggest that type II afferents sense loud, potentially damaging levels of sound. To explore this hypothesis further, calcium imaging was used to determine the impact of acoustic trauma on the activity of type II cochlear afferents of young adult mice of both sexes. Two known marker genes (Th, Drd2) and one new marker gene (Tac1), expressed in type II afferents and some other cochlear cell types, drove GCaMP6f expression to reveal calcium transients in response to focal damage in the organ of Corti in all turns of the cochlea. Mature type II afferents responded to acute photoablation damage less often but at greater length compared with prehearing neurons. In addition, days after acoustic trauma, acute photoablation triggered a novel response pattern in type II afferents and surrounding epithelial cells, delayed bursts of activity occurring minutes after the initial response subsided. Overall, calcium imaging can report type II afferent responses to damage even in mature and noise-exposed animals and reveals previously unknown tissue hyperactivity subsequent to acoustic trauma.