To hum or not to hum: Neural transcriptome signature of male courtship vocalization in a teleost fish. (9th June 2021)

• Record Type: Journal Article
• Authors: Tripp, Joel A.; Feng, Ni Y.; Bass, Andrew H.
• Is Part Of: Genes, brain, and behavior. Volume 20:Number 6(2021)
• Page Start: n/a
• Page End: n/a
• Publication Date: 2021-06-09
• Subjects: aromatase -- clock genes -- hypothalamus -- ion channel -- metabolism -- motoneuron -- preoptic area -- synaptic transmission -- transcriptome -- vocalization; Behavior genetics -- Periodicals; Neurogenetics -- Periodicals; 616.8
• DOI: 10.1111/gbb.12740
• Languages: English
• ISSNs: 1601-1848

Abstract

Abstract: For many animal species, vocal communication is a critical social behavior and often a necessary component of reproductive success. Additionally, vocalizations are often demanding motor acts. Wanting to know whether a specific molecular toolkit might be required for vocalization, we used RNA‐sequencing to investigate neural gene expression underlying the performance of an extreme vocal behavior, the courtship hum of the plainfin midshipman fish ( Porichthys notatus ). Single hums can last up to 2 h and may be repeated throughout an evening of courtship activity. We asked whether vocal behavioral states are associated with specific gene expression signatures in key brain regions that regulate vocalization by comparing transcript expression levels in humming versus non‐humming males. We find that the circadian‐related genes period3 and Clock are significantly upregulated in the vocal motor nucleus and preoptic area‐anterior hypothalamus, respectively, in humming compared with non‐humming males, indicating that internal circadian clocks may differ between these divergent behavioral states. In addition, we identify suites of differentially expressed genes related to synaptic transmission, ion channels and transport, neuropeptide and hormone signaling, and metabolism and antioxidant activity that together may support the neural and energetic demands of humming behavior. Comparisons of transcript expression across regions stress regional differences in brain gene expression, while also showing coordinated gene regulation in the vocal motor circuit in preparation for courtship behavior. These results underscore the role of differential gene expression in shifts between behavioral states, in this case neuroendocrine, motor and circadian control of courtship vocalization. Abstract : Vocalization is a critical social behavior for many species. We examined brain transcriptome changes during production of an extreme vocal behavior, the courtship hums of plainfin midshipman fish. Hums are simple acoustically but feature extraordinary duration and motoneuronal synchrony. Focusing on the forebrain preoptic area‐anterior hypothalamus and the hindbrain vocal motor nucleus, we found hum‐dependent expression of transcripts related to circadian rhythm, synaptic transmission, ion channels, metabolism, and neuropeptide and hormone signaling. Though expression was strongly influenced by brain region, behavioral state‐dependent differentially expressed transcripts were largely concordant across brain regions. Our results emphasize the importance of circadian control of social vocalization, identify new candidate genes for vocal behavior regulation, and suggest a common molecular toolkit in vocal circuits.