The neurobiology of sensing respiratory gases for the control of animal behavior

doi:10.1007/s11515-012-1219-x

Front Biol

2012, Vol. 7

Issue (3) : 246-253 https://doi.org/10.1007/s11515-012-1219-x

REVIEW

The neurobiology of sensing respiratory gases for the control of animal behavior

Dengke K. MA¹(

), Niels RINGSTAD²(

)

1. Department of Biology, McGovern Institute for Brain Research, MIT, Cambridge, MA 02139, USA.; 2. Department of Cell Biology and the Helen L. and Martin S. Kimmel Center for Biology and Medicine at the Skirball Institute of Biomolecular Medicine, New York University Langone Medical Center, New York, NY 10016, USA

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Abstract

Aerobic metabolism is fundamental for almost all animal life. Cellular consumption of oxygen (O₂) and production of carbon dioxide (CO₂) signal metabolic states and physiologic stresses. These respiratory gases are also detected as environmental cues that can signal external food quality and the presence of prey, predators and mates. In both contexts, animal nervous systems are endowed with mechanisms for sensing O₂/CO₂ to trigger appropriate behaviors and maintain homeostasis of internal O₂/CO₂. Although different animal species show different behavioral responses to O₂/CO₂, some underlying molecular mechanisms and pathways that function in the detection of respiratory gases are fundamentally similar and evolutionarily conserved. Studies of Caenorhabditis elegans and Drosophila melanogaster have identified roles for cyclic nucleotide signaling and the hypoxia inducible factor (HIF) transcriptional pathway in mediating behavioral responses to respiratory gases. Understanding how simple invertebrate nervous systems detect respiratory gases to control behavior might reveal general principles common to nematodes, insects and vertebrates that function in the molecular sensing of respiratory gases and the neural control of animal behaviors.

Keywords oxygen carbon dioxide C. elegans Drosophila respiratory gases animal behaviors

Corresponding Author(s): MA Dengke K.,Email:dkma@mit.edu; RINGSTAD Niels,Email:niels.ringstad@med.nyu.edu

Issue Date: 01 June 2012

Cite this article:

Dengke K. MA,Niels RINGSTAD. The neurobiology of sensing respiratory gases for the control of animal behavior[J]. Front Biol, 2012, 7(3): 246-253.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1219-x
https://academic.hep.com.cn/fib/EN/Y2012/V7/I3/246

Fig.1 Schematic molecular mechanisms of sensing O or CO levels to direct acute behavioral or homeostatic responses in and vertebrates. In both and , sensing changes in O levels to direct acute behavioral responses is mediated by atypical nucleotide guanylate cyclases (GCs) that can bind O, which regulates the enzymatic activity of GCs to convert GTP to cyclic GMP. In vertebrates, sensing reduction in O levels to direct ventilation responses in the carotid body appears to be mediated by HS, which increases in levels upon hypoxia. There are also acute behaviors that require mechanisms independently of cyclic nucleotides in and it remains unknown whether vertebrates also use GCs to modulate ventilation. Sensing changes in CO levels in both and vertebrates appears to be mainly mediated by GCs and/or adenylate cyclases (ACs); whether it is also the case in remains to be seen. The perception of carbonation in mammals uses pH-sensing mechanisms via carbonic anhydrase (CA)-generated protons. In all animal species examined so far, an evolutionarily conserved transcriptional pathway mediates the homeostatic response to hypoxia. The O-sensing hydroxylase EGLN family proteins is modulated by antagonizing actions of O and HS to inhibit HIF transcription factors, which ultimately direct adaptive responses to hypoxia by the transcriptional regulation of its numerous target genes.

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