Neuroendocrine control of seasonal plasticity in the auditory and vocal systems of fish

Abstract

Seasonal changes in reproductive-related vocal behavior are widespread among fishes. This review highlights recent studies of the vocal plainfin midshipman fish, Porichthys notatus, a neuroethological model system used for the past two decades to explore neural and endocrine mechanisms of vocal-acoustic social behaviors shared with tetrapods. Integrative approaches combining behavior, neurophysiology, neuropharmacology, neuroanatomy, and gene expression methodologies have taken advantage of simple, stereotyped and easily quantifiable behaviors controlled by discrete neural networks in this model system to enable discoveries such as the first demonstration of adaptive seasonal plasticity in the auditory periphery of a vertebrate as well as rapid steroid and neuropeptide effects on vocal physiology and behavior. This simple model system has now revealed cellular and molecular mechanisms underlying seasonal and steroid-driven auditory and vocal plasticity in the vertebrate brain.

FoxP2 Expression in a Highly Vocal Teleost Fish with Comparisons to Tetrapods

“…The current study maps FoxP2 mRNA expression in the brain of the highly vocal plainfin midshipman (Porichthys notatus) that has been the subject of comprehensive mapping of the central vocal, auditory, and neuroendocrine systems that modulate vocal-acoustic behaviors [ Fig. 1; see reviews in Bass, 2014;Forlano et al, 2015;Feng and Bass, 2017]. Comparison of the brain expression pattern of FoxP2 in midshipman with findings in other teleosts, as well as in mice and birds, suggests a pattern of evolutionarily conserved FoxP2-expressing brain regions.…”

Seasonal plasticity of auditory saccular sensitivity in “sneaker” type II male plainfin midshipman fish, Porichthys notatus

“…5). Nesting type I males produce three types of acoustic signals that include agonistic grunts and growls and advertisement calls known as hums Forlano et al 2015). Reproductive type I males often produce trains of broadband, short-duration (50-200 ms) grunts (Fig.…”

“…In addition, Coffin et al (2012) also observed in reproductive females that the increase in saccular hair cell density was concurrent with increases in overall magnitude of the evoked saccular potentials and decreases in auditory saccular thresholds (.i.e., increased auditory sensitivity). The above-mentioned mechanisms potentially responsible for the observed seasonal changes in saccular sensitivity have been proposed to be induced by estrogens and androgens acting via long term signaling pathways to upregulate BK channels and modulate hair cell proliferation and death to ultimately enhance the hearing sensitivity in this species (Coffin et al 2012;Forlano et al 2015Forlano et al , 2016. However, this steroid-mediated mechanism hypothesis remains to be tested.…”

“…Recent studies have shown that many teleosts possess both behavioral and neural adaptations for the production and perception of acoustic signals that are necessary for reproduction and survival (Bass and McKibben 2003;Bass and Ladich 2008;Kelley and Bass 2010). One vocal teleost that is a good species for investigating neural mechanisms of vocal production and signal perception is the plainfin midshipman fish, Porichthys notatus Sisneros 2009a;Forlano et al 2015). This nocturnally active marine teleost produces a relatively simple repertoire of acoustic signals for intraspecific social communication that includes "grunts", "growls" and "hums" Sisneros 2009a).…”

Sex differences and endocrine regulation of auditory-evoked, neural responses in African clawed frogs (Xenopus)

“…The onset latency of the threshold responses (3 – 5 ms) suggests that they reflect auditory nerve activity. Thus, loci for androgen action could be the hair cells in the auditory periphery (Forlano et al 2015), or neurons in the acoustic ganglion expressing androgen receptor (Perez et al 1996). Androgens contribute to feminization or have female-specific effects in other species and are the primary steroid produced in the Xenopus ovary (Lutz et al 2001).…”