Melatonin receptor expression in vocal, auditory, and neuroendocrine centers of a highly vocal fish, the plainfin midshipman (Porichthys notatus)

Abstract

Melatonin plays a central role in entraining activity to the day–night cycle in vertebrates. Here, we investigate neuroanatomical substrates of melatonin‐dependent vocal–acoustic behavior in the nocturnal and highly vocal teleost fish, the plainfin midshipman (Porichthys notatus). Using in situ hybridization (ISH) and quantitative real‐time PCR (qPCR), we assess the mRNA distribution and transcript abundance of melatonin receptor subtype 1B (mel1b), shown to be important for vocalization in midshipman fish and songbirds. ISH shows robust mel1b expression in major nodes of the central vocal and auditory networks in the subpallium, preoptic area (POA), anterior hypothalamus, dorsal thalamus, posterior tuberculum, midbrain torus semicircularis and periaqueductal gray, and hindbrain. Mel1b label is also abundant in secondary targets of the olfactory, visual, and lateral line systems, as well as telencephalic regions that have been compared to the amygdala, extended amygdala, striatum, septum, and hippocampus of tetrapods. Q‐PCR corroborates mel1b abundance throughout the brain and shows significant increases in the morning compared with nighttime in tissue samples inclusive of the telencephalon and POA, but remains stable in other brain regions. Plasma melatonin levels show expected increase at night. Our findings support the hypothesis that melatonin's stimulatory effects on vocal–acoustic mechanisms in midshipman is mediated, in part, by melatonin binding in vocal, auditory, and neuroendocrine centers. Together with robust mel1b expression in multiple telencephalic nuclei and sensory systems, the results further indicate an expression pattern comparable to that in birds and mammals that is indicative of melatonin's broad involvement in the modulation of physiology and behavior.

Galanin immunoreactivity is sexually polymorphic in neuroendocrine and vocal‐acoustic systems in a teleost fish

“…Figure a indicates the approximate levels along the rostral‐caudal axis that are illustrated in Figures (levels for 2c, 3e, and 4e correspond to levels shown in Figure ; see legend for Figure ), and includes representative Nissl‐stained sections from non‐experimental material that provide more cytoarchitectural detail of the regions illustrated in Figures . The nomenclature used here largely follows that used in prior publications on midshipman fish (e.g., Feng et al, ) and zebrafish (Wullimann, Rupp, & Reichert, ).…”

“…To better localize the neuronal populations where Gal might act to influence performance of the above behaviors, we sought to determine if and how Gal‐ir systems in the midshipman brain differ within and between the sexes. Complementing prior neuroanatomical studies of midshipman (Feng, Marchaterre, & Bass, ; Forlano, Deitcher, & Bass, ; Forlano, Marchaterre, Deitcher, & Bass, ; Goodson & Bass, ; Goodson, Evans, & Bass, ) our analysis of Gal neuroanatomy focuses on the well‐established vocal‐acoustic (Figure ) and neuroendocrine circuitry by addressing four questions: (1) Where are Gal‐ir neurons and their projections distributed in the brain? (2) Does the pattern of Gal expression differ between the two male morphs and females?…”

To hum or not to hum: Neural transcriptome signature of courtship vocalization in a teleost fish

“…Only a single transcript related to hormone signaling, pro-FMRFamide-related neuropeptide FF was differentially expressed between humming and non-humming midshipman males. This result was surprising because the POA-AH has dense expression of neuropeptides and hormone receptors—including arginine-vasotocin (AVT) and isotocin (teleost homologues of mammalian arginine-vasopressin and oxytocin, respectively) and their receptors, galanin, stress-related peptides (corticotropin-releasing hormone and urocortin-3), somatotropin, androgen and estrogen receptors, the enzyme aromatase which converts testosterone to estradiol, as well as a receptor for the hormone melatonin, which promotes vocalization 8,15,18,19,39,40,43–46 . Further, hormone signaling was the single significantly enriched GO term in our study of the POA-AH during spawning 15 .…”

“…We used RNA-sequencing (RNAseq) to identify transcriptional changes that occur during humming in both the VMN and POA-AH of type I male midshipman. We found that the vocally active behavioral state of humming is characterized by differential expression of a suite of functionally important genes supporting synaptic transmission, ion channels and transport, hormone signaling, and metabolism and antioxidant activity—categories that have been the focus of earlier studies of vocalization in midshipman or have been associated with courtship vocalization 5,15,18,19 . We also found that the circadian genes period3 ( per3 ) and circadian locomotor output cycles kaput-like ( Clock ) were differentially expressed between humming and non-humming males in the VMN and POA-AH, respectively; an unexpected but exciting result given that midshipman vocalization is under circadian control 8 .…”

Melatonin and osmoregulation in fish: A focus on Atlantic salmon Salmo salar smoltification

“…Duplicates of some of these receptors are found in some fish species,121,[123][124][125][126] probably as a consequence of the gains and losses resulting from the teleost specific and salmonid specific whole genome duplications 127. As expected, the receptors display distinct binding characteristics for melatonin or melatonin analogues (e.g., O. latipes122 and S. salar 128 ) when tested in heterologous cell lines.One remarkable feature of melatonin receptors is their wide distribution in central and peripheral tissues [122][123][124][125][128][129][130][131][132][133][134][135][136][137][138][139][140][141][142]. Nervous tissues expressing these receptors include the brain, the retina and the pineal gland itself.…”