Abstract
In seasonal breeding vertebrates, hormone regulation of catecholamines, which include dopamine and noradrenaline, may function, in part, to modulate behavioral responses to conspecific vocalizations. However, natural seasonal changes in catecholamine innervation of auditory nuclei is largely unexplored, especially in the peripheral auditory system, where encoding of social acoustic stimuli is initiated. The plainfin midshipman fish, Porichthys notatus, has proven to be an excellent model to explore mechanisms underlying seasonal peripheral auditory plasticity related to reproductive social behavior. Recently, we demonstrated robust catecholaminergic (CA) innervation throughout the auditory system in midshipman. Most notably, dopaminergic neurons in the diencephalon have widespread projections to auditory circuitry including direct innervation of the saccule, the main endorgan of hearing, and the cholinergic octavolateralis efferent nucleus (OE) which also projects to the inner ear. Here, we tested the hypothesis that gravid, reproductive summer females show differential CA innervation of the auditory system compared to non-reproductive winter females. We utilized quantitative immunofluorescence to measure tyrosine hydroxylase immunoreactive (TH-ir) fiber density throughout central auditory nuclei and the sensory epithelium of the saccule. Reproductive females exhibited greater density of TH-ir innervation in two forebrain areas including the auditory thalamus and greater density of TH-ir on somata and dendrites of the OE. In contrast, non-reproductive females had greater numbers of TH-ir terminals in the saccule and greater TH-ir fiber density in a region of the auditory hindbrain as well as greater numbers of TH-ir neurons in the preoptic area. These data provide evidence that catecholamines may function, in part, to seasonally modulate the sensitivity of the inner ear and, in turn, the appropriate behavioral response to reproductive acoustic signals.
Highlights
Catecholamines are well documented as important regulators of reward and motivated social behavior, but are known modulators of sensory and motor systems [1,2,3]
We showed that males exposed to advertisement calls of other males exhibit a cFos response in TPp tyrosine hydroxylase immunoreactivity (TH-ir) neurons which are active in response to social acoustic cues [40]
Average body size measured by standard length (SL) was largely overlapping between seasons, but summer females were approximately 9.1% larger on average than winter females (t(10) = 2.989, p = 0.0136)
Summary
Catecholamines are well documented as important regulators of reward and motivated social behavior, but are known modulators of sensory and motor systems [1,2,3]. Largely in songbirds, provide strong evidence that both dopamine and noradrenaline are important neuromodulators of vocal-acoustic communication, especially in the context of appropriate brain and behavioral response to social auditory signals (for review see [4]). Hormone regulation of catecholaminergic (CA) innervation of sensory areas may be a conserved mechanism for differential seasonal response to conspecific vocalizations [5, 6]. In support of this, mimicking seasonal changes in circulating steroid levels has provided evidence that estrogen increases CA innervation of midbrain and forebrain auditory nuclei in female white-throated sparrows as measured by changes in tyrosine hydroxylase immunoreactivity (TH-ir) [7, 8]. The plainfin midshipman fish, Porichthys notatus, has proven to be an excellent model to explore mechanisms underlying seasonal plasticity in audition related to reproductive social behavior [9,10,11]. Females find nesting males by localizing the source of the hum, deposit their eggs in a single nest and head back offshore while the male cares for the young and continues to court other females until the nest is full of developing embryos [10, 12, 13]
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