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