Forebrain Dopamine System Regulates Inner Ear Auditory Sensitivity to Socially Relevant Acoustic Signals

Abstract

Dopamine is integral to attentional and motivational processes, but studies are largely restricted to the central nervous system. In mammals [1, 2] and fishes [3, 4], central dopaminergic neurons project to the inner ear and could modulate acoustic signals at the earliest stages of processing. Studies in rodents show dopamine inhibits cochlear afferent neurons and protects against noise-induced acoustic injury [5-10]. However, other functions for inner ear dopamine have not been investigated, and the effect of dopamine on peripheral auditory processing in non-mammalians remains unknown [11, 12]. Insights could be gained by studies conducted in the context of intraspecific acoustic communication. We present evidence from a vocal fish linking reproductive-state-dependent changes in auditory sensitivity with seasonal changes in the dopaminergic efferent system in the saccule, their primary organ of hearing. Plainfin midshipman (Porichthys notatus) migrate from deep-water winter habitats to the intertidal zone in the summer to breed. Nesting males produce nocturnal vocalizations to attract females [13]. Both sexes undergo seasonal enhancement of hearing sensitivity at the level of the hair cell [14-16], increasing the likelihood of detecting conspecific signals [17, 18]. Importantly, reproductive females concurrently have reduced dopaminergic input to the saccule [19]. Here, we show that dopamine decreases saccule auditory sensitivity via a D2-like receptor. Saccule D2a receptor expression is reduced in the summer and correlates with sensitivity within and across seasons. We propose that reproductive-state-dependent changes to the dopaminergic efferent system provide a release of inhibition in the saccule, enhancing peripheral encoding of social-acoustic signals.

Keywords: acoustic; auditory; communication; dopamine; dopaminergic; efferent; fish; hair cell; hearing; inner ear.