Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats

Freezing, a characteristic pattern of defensive behavior elicited by fear, is associated with a decrease in the heart rate. Central mechanisms underlying fear bradycardia are poorly understood. The periaqueductal gray (PAG) in the midbrain is known to contribute to autonomic cardiovascular adjustmen...

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Main Authors:	Koba, Satoshi, Inoue, Ryo, Watanabe, Tatsuo
Format:	Online
Language:	English
Published:	John Wiley and Sons Inc. 2016
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4923232/

id	pubmed-4923232
recordtype	oai_dc
spelling	pubmed-49232322016-07-06 Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats Koba, Satoshi Inoue, Ryo Watanabe, Tatsuo Original Research Freezing, a characteristic pattern of defensive behavior elicited by fear, is associated with a decrease in the heart rate. Central mechanisms underlying fear bradycardia are poorly understood. The periaqueductal gray (PAG) in the midbrain is known to contribute to autonomic cardiovascular adjustments associated with various emotional behaviors observed during active or passive defense reactions. The purpose of this study was to elucidate the role played by PAG neurons in eliciting fear bradycardia. White noise sound (WNS) exposure at 90 dB induced freezing behavior and elicited bradycardia in conscious rats. The WNS exposure‐elicited bradycardia was mediated parasympathetically because intravenous administration of atropine abolished the bradycardia (P < 0.05). Moreover, WNS exposure‐elicited bradycardia was mediated by neuronal activation of the lateral/ventrolateral PAG (l/vlPAG) because bilateral microinjection of muscimol, a GABAA agonist, into the l/vlPAG significantly suppressed the bradycardia. It is noted that muscimol microinjected bilaterally into the dorsolateral PAG had no effect on WNS exposure‐elicited bradycardia. Furthermore, retrograde neuronal tracing experiments combined with immunohistochemistry demonstrated that a number of l/vlPAG neurons that send direct projections to the nucleus ambiguus (NA) in the medulla, a major origin of parasympathetic preganglionic neurons to the heart, were activated by WNS exposure. Based on these findings, we propose that the l/vlPAG‐NA monosynaptic pathway transmits fear‐driven central signals, which elicit bradycardia through parasympathetic outflow. John Wiley and Sons Inc. 2016-06-22 /pmc/articles/PMC4923232/ /pubmed/27335434 http://dx.doi.org/10.14814/phy2.12831 Text en © 2016 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Koba, Satoshi Inoue, Ryo Watanabe, Tatsuo
spellingShingle	Koba, Satoshi Inoue, Ryo Watanabe, Tatsuo Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
author_facet	Koba, Satoshi Inoue, Ryo Watanabe, Tatsuo
author_sort	Koba, Satoshi
title	Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
title_short	Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
title_full	Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
title_fullStr	Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
title_full_unstemmed	Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
title_sort	role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
description	Freezing, a characteristic pattern of defensive behavior elicited by fear, is associated with a decrease in the heart rate. Central mechanisms underlying fear bradycardia are poorly understood. The periaqueductal gray (PAG) in the midbrain is known to contribute to autonomic cardiovascular adjustments associated with various emotional behaviors observed during active or passive defense reactions. The purpose of this study was to elucidate the role played by PAG neurons in eliciting fear bradycardia. White noise sound (WNS) exposure at 90 dB induced freezing behavior and elicited bradycardia in conscious rats. The WNS exposure‐elicited bradycardia was mediated parasympathetically because intravenous administration of atropine abolished the bradycardia (P < 0.05). Moreover, WNS exposure‐elicited bradycardia was mediated by neuronal activation of the lateral/ventrolateral PAG (l/vlPAG) because bilateral microinjection of muscimol, a GABAA agonist, into the l/vlPAG significantly suppressed the bradycardia. It is noted that muscimol microinjected bilaterally into the dorsolateral PAG had no effect on WNS exposure‐elicited bradycardia. Furthermore, retrograde neuronal tracing experiments combined with immunohistochemistry demonstrated that a number of l/vlPAG neurons that send direct projections to the nucleus ambiguus (NA) in the medulla, a major origin of parasympathetic preganglionic neurons to the heart, were activated by WNS exposure. Based on these findings, we propose that the l/vlPAG‐NA monosynaptic pathway transmits fear‐driven central signals, which elicit bradycardia through parasympathetic outflow.
publisher	John Wiley and Sons Inc.
publishDate	2016
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4923232/
_version_	1613600339948208128

Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats

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