Connectivity and ultrastructure of dopaminergic innervation of the inner ear and auditory efferent system of a vocal fish

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Efferent control is an important feature of sensory systems but remains less well understood than afferent pathways. Nearly all vertebrates examined to date possess a cholinergic efferent innervation of the inner ear that originates in the hindbrain (Köppl, 2011), with proposed functions that include protection from overstimulation, homeostasis, selective attention, signal detection, and sound source localization (Andéol et al., 2011; Darrow, Maison, & Liberman, 2006; Robertson, 2009; Smith & Keil, 2015; Terreros, Jorratt, Aedo, Elgoyhen, & Delano, 2016; Tomchik & Lu, 2006b). While cholinergic auditory efferents are well studied across vertebrate taxa, comparatively less attention has been given to dopamine (DA) as a modulator of peripheral hearing (Gil‐Loyzaga, 1995). DA fibers and receptors have been localized within the rodent cochlea (Darrow, Simons, Dodds, & Liberman, 2006; Maison et al., 2012), but studies examining DA innervation of auditory endorgans of anamniotes are limited to a single species of teleost fish (Forlano, Kim, Krzyminska, & Sisneros, 2014; Forlano, Ghahramani et al., 2015) and investigations of the ultrastructure of DA terminals are limited to guinea pig (d'Aldin et al., 1995; Eybalin, Charachon, & Renard, 1993). The function of DA in the cochlea, as suggested by studies in rodents, is to protect against acoustic trauma (Lendvai et al., 2011; Maison et al., 2012; Ruel et al., 2001), but other hypotheses, such as signal detection and sound source localization, have not been tested. The potential modulatory role of DA in the auditory periphery in the context of natural behaviors remains unexplored.
The plainfin midshipman fish, Porichthys notatus, is an excellent model organism for investigating neural mechanisms of vocal‐acoustic behavior, with well‐characterized ascending and descending auditory pathways (Bass, Bodnar, & Marchaterre, 2000; Bass, Marchaterre, & Baker, 1994; Goodson & Bass, 2002). During the summer breeding season, type I males migrate from the benthic zone to intertidal nesting sites along the northwestern coast of North America where they produce nocturnal hum‐like vocalizations that attract females for mating opportunities. Type II males do not build nests or court females but rather sneak fertilization opportunities (Bass, 1996; Brantley & Bass, 1994). All adult morphs (type Is, females and type II males) undergo seasonal and steroid dependent changes in the auditory periphery, resulting in lower hearing thresholds and improved encoding of social signals in the summer, specifically within the range of the upper harmonics of the male vocalization (Bhandiwad, Whitchurch, Colleye, Zeddies, & Sisneros, 2017; Forlano, Maruska, Sisneros, & Bass, 2016; Rohmann & Bass, 2011; Sisneros & Bass, 2003; Sisneros, Forlano, Deitcher, & Bass, 2004). This likely improves detection of the courtship call, as the upper harmonics propagate farther in the shallow water of the intertidal zone (Bass & Clark, 2003; Fine & Lenhardt, 1983). Mechanisms for this plasticity include an increase in the number of sensory receptors, that is, hair cells, in the inner ear (Coffin, Mohr, & Sisneros, 2012), as well an upregulation in the number of calcium‐activated potassium (BK) channels in hair cells (Rohmann, Fergus, & Bass, 2013). It has also been suggested that centrifugal modulation could mediate plasticity (Forlano, Sisneros, Rohmann, & Bass, 2015; Sisneros & Bass, 2003). The saccule, the main endorgan of hearing in midshipman (Cohen & Winn, 1967) and most teleosts (Popper & Fay, 1999), receives tyrosine hydroxylase (TH, enzyme for catecholaminergic synthesis) innervation from the periventricular posterior tuberculum (TPp) in the diencephalon (Forlano et al., 2014, Figure 1a, b), a proposed homolog of the mammalian A11 DA cell group (Schweitzer, Lohr, Filippi, & Driever, 2012; Yamamoto & Vernier, 2011). The saccule also receives cholinergic efferent innervation from the octavolateralis efferent nucleus (OE) in the hindbrain (Bass et al.
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