Hormonal regulation of thirst in the amphibious ray-finned fish suggests the requirement for terrestrialization during evolution
Open Access
- 8 November 2019
- journal article
- research article
- Published by Springer Nature in Scientific Reports
- Vol. 9 (1) , 1-10
Abstract
Thirst has evolved for vertebrate terrestrial adaptation. We previously showed that buccal drying induced a series of drinking behaviours (migration to water–taking water into the mouth–swallowing) in the amphibious mudskipper goby, thereby discovering thirst in ray-finned fish. However, roles of dipsogenic/antidipsogenic hormones, which act on the thirst center in terrestrial tetrapods, have remained unclear in the mudskipper thirst. Here we examined the hormonal effects on the mudskipper drinking behaviours, particularly the antagonistic interaction between angiotensin II (AngII) and atrial natriuretic peptide (ANP) which is important for thirst regulation in mammalian ‘forebrain’. Expectedly, intracerebroventricular injection of ANP in mudskippers reduced AngII-increased drinking rate. ANP also suppressed the neural activity at the ‘hindbrain’ region for the swallowing reflex, and the maintenance of buccopharyngeal water due to the swallowing inhibition may attenuate the motivation to move to water. Thus, the hormonal molecules involved in drinking regulation, as well as the influence of buccopharyngeal water, appear to be conserved in distantly related species to solve osmoregulatory problems, whereas hormonal control of thirst at the forebrain might have been acquired only in tetrapod lineage during evolution.Keywords
Funding Information
- MEXT | Japan Society for the Promotion of Science (JP 16J01114)
This publication has 51 references indexed in Scilit:
- The Cells and Circuitry for Itch Responses in MiceScience, 2013
- The area postrema in hindbrain is a central player for regulation of drinking behavior in Japanese eelsAmerican Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 2011
- “Blood‐contacting neurons” in the brain of the Japanese eel Anguilla japonicaJournal of Experimental Zoology Part A: Comparative Experimental Biology, 2005
- Medullary motor neurones associated with drinking behaviour of Japanese eelsJournal of Fish Biology, 2003
- Biological characterization of human brain natriuretic peptide (BNP) and rat BNP: Species-specific actions of BNPBiochemical and Biophysical Research Communications, 1990
- Atrial natriuretic peptide in the subfornical organ reduces drinking induced by angiotensin or in response to water deprivation.Behavioral Neuroscience, 1990
- Atrial natriuretic peptide in the subfornical organ reduces drinking induced by angiotensin or in response to water deprivation.Behavioral Neuroscience, 1990
- Atrial natriuretic polypeptide depresses angiotensin II induced excitation of neurons in the rat subfornical organ in vitroBrain Research, 1988
- Area postrema of the goldfish, Carassius auratus: Ultrastructure, fiber connections, and immunocytochemistryJournal of Comparative Neurology, 1987
- Terrestrial feeding in the Mudskipper Periophthalmus (Pisces: Teleostei): A cineradiographic analysisJournal of Zoology, 1981