Exposure to Advertisement Calls of Reproductive Competitors Activates Vocal-Acoustic and Catecholaminergic Neurons in the Plainfin Midshipman Fish, Porichthys notatus

Abstract

While the neural circuitry and physiology of the auditory system is well studied among vertebrates, far less is known about how the auditory system interacts with other neural substrates to mediate behavioral responses to social acoustic signals. One species that has been the subject of intensive neuroethological investigation with regard to the production and perception of social acoustic signals is the plainfin midshipman fish, Porichthys notatus, in part because acoustic communication is essential to their reproductive behavior. Nesting male midshipman vocally court females by producing a long duration advertisement call. Females localize males by their advertisement call, spawn and deposit all their eggs in their mate’s nest. As multiple courting males establish nests in close proximity to one another, the perception of another male’s call may modulate individual calling behavior in competition for females. We tested the hypothesis that nesting males exposed to advertisement calls of other males would show elevated neural activity in auditory and vocal-acoustic brain centers as well as differential activation of catecholaminergic neurons compared to males exposed only to ambient noise. Experimental brains were then double labeled by immunofluorescence (-ir) for tyrosine hydroxylase (TH), an enzyme necessary for catecholamine synthesis, and cFos, an immediate-early gene product used as a marker for neural activation. Males exposed to other advertisement calls showed a significantly greater percentage of TH-ir cells colocalized with cFos-ir in the noradrenergic locus coeruleus and the dopaminergic periventricular posterior tuberculum, as well as increased numbers of cFos-ir neurons in several levels of the auditory and vocal-acoustic pathway. Increased activation of catecholaminergic neurons may serve to coordinate appropriate behavioral responses to male competitors. Additionally, these results implicate a role for specific catecholaminergic neuronal groups in auditory-driven social behavior in fishes, consistent with a conserved function in social acoustic behavior across vertebrates.

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…18; Goodson and Kingsbury, 2013;2012;Petersen et al, 2013). Interestingly, ~ 8% of TPp TH-ir cells in male midshipman were colabeled with cFos-ir after mate call playback (Petersen et al, 2013) which approximates the number of TH-ir neurons that project to the saccule (current study).…”

“…In addition, there were significant positive correlations between numbers of cFos-ir at all levels of the auditory system we investigated (DOri, TSnc, CP and AT) and percent colocalization of cFos in TH-ir LC neurons (Petersen et al, 2013) which may reflect LC connectivity to those areas (see Hoke et al, 2005). The LC may receive direct and/or indirect auditory input as both the TS and PAG send projections to the corresponding isthmal region in midshipman Kittelberger and Bass, 2013), although whether contacts are made on LC neurons would require confirmation by double-label experiments.…”

“…In midshipman there are several hundred neurons of this type (Petersen et al, 2013), which far outnumber the few documented in zebrafish adults (Ma, 2003;Rink and Wullimann, 2001). These distinctive TH-ir neurons correspond to those reported as paraventricular organ-accompanying (PVOa), magnocellular hypothalamic nucleus, or nucleus of the TPp (nTPp) cells located lateral to the anterior PVO described in other teleosts (Ma, 2003;Meek, 1994;Meek and Nieuwenhuys, 1998;Rink and Wullimann, 2001;2002b).…”

“…Since some of those same neurons may not only project to the saccule and hindbrain auditory nuclei, but also send ascending projections to the ventral telencephalon (i.e., Vd, Vv; see Wullimann, 2001, 2002;Tay et al, 2011), these dopaminergic neurons in the TPp are in a perfect position to affect primary auditory processing and higher brain function involved in behavioral decision making to salient auditory cues ( Fig. 18; Goodson and Kingsbury, 2013;2012;Petersen et al, 2013). Interestingly, ~ 8% of TPp TH-ir cells in male midshipman were colabeled with cFos-ir after mate call playback (Petersen et al, 2013) which approximates the number of TH-ir neurons that project to the saccule (current study).…”

“…Regardless of homology, the widespread projection pattern (largely descending but also ascending) of these TPp neurons position them to be important integrative neuromodulators of sensory and motor function, cognition and behavior (Ma, 2003;Schweitzer et al, 2012;Tay et al, 2011). Teleosts exhibit CA neuronal populations and innervation patterns in nuclei with proposed homologies to those found in tetrapods where they are known to modulate motivated social and reproductive behavior (Goodson and Kingsbury, 2013;Petersen et al, 2013). However, aside from DA neurons in the anterior preoptic area that are well documented to regulate the hypothalamic-pituitary-gonadal (HPG) axis in teleosts (Dufour et al, 2010;Dufour et al, 2005;Kah et al, 1987;Peter and Fryer, 1983), the function of specific CA cell groups in teleosts are largely unknown.…”