PreBötzinger complex neurons drive respiratory modulation of blood pressure and heart rate

Clément Menuet; Angela A. Connelly; Jaspreet K. Bassi; Mariana R. Melo; Sheng Le; Jessica Kamar; Natasha N. Kumar; Stuart J. McDougall; Simon McMullan; Andrew M. Allen

doi:10.7554/eLife.57288

PreBötzinger complex neurons drive respiratory modulation of blood pressure and heart rate

Clément Menuet, Angela A. Connelly, Jaspreet K. Bassi, Mariana R. Melo, Sheng Le, Jessica Kamar, Natasha N. Kumar, Stuart J. McDougall, Simon McMullan, Andrew M. Allen

Faculty of Medicine, Health and Human Sciences

Research output: Contribution to journal › Article › peer-review

54 Citations (Scopus)

68 Downloads (Pure)

Abstract

Heart rate and blood pressure oscillate in phase with respiratory activity. A component of these oscillations is generated centrally, with respiratory neurons entraining the activity of pre-sympathetic and parasympathetic cardiovascular neurons. Using a combination of optogenetic inhibition and excitation in vivo and in situ in rats, as well as neuronal tracing, we demonstrate that preBötzinger Complex (preBötC) neurons, which form the kernel for inspiratory rhythm generation, directly modulate cardiovascular activity. Specifically, inhibitory preBötC neurons modulate cardiac parasympathetic neuron activity whilst excitatory preBötC neurons modulate sympathetic vasomotor neuron activity, generating heart rate and blood pressure oscillations in phase with respiration. Our data reveal yet more functions entrained to the activity of the preBötC, with a role in generating cardiorespiratory oscillations. The findings have implications for cardiovascular pathologies, such as hypertension and heart failure, where respiratory entrainment of heart rate is diminished and respiratory entrainment of blood pressure exaggerated.

Original language	English
Article number	e57288
Pages (from-to)	1-30
Number of pages	30
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.57288
Publication status	Published - 15 Jun 2020

Bibliographical note

Copyright the Author(s). Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

cardiorespiratory control
master oscillator
neuroscience
optogenetic inhibition
prebötzinger complex
rat
respiratory sinus arrhythmia
respiratory-sympathetic modulation

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10.7554/eLife.57288Licence: CC BY

Publisher version (open access)Final published version, 9.55 MBLicence: CC BY

Cite this

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title = "PreB{\"o}tzinger complex neurons drive respiratory modulation of blood pressure and heart rate",

abstract = "Heart rate and blood pressure oscillate in phase with respiratory activity. A component of these oscillations is generated centrally, with respiratory neurons entraining the activity of pre-sympathetic and parasympathetic cardiovascular neurons. Using a combination of optogenetic inhibition and excitation in vivo and in situ in rats, as well as neuronal tracing, we demonstrate that preB{\"o}tzinger Complex (preB{\"o}tC) neurons, which form the kernel for inspiratory rhythm generation, directly modulate cardiovascular activity. Specifically, inhibitory preB{\"o}tC neurons modulate cardiac parasympathetic neuron activity whilst excitatory preB{\"o}tC neurons modulate sympathetic vasomotor neuron activity, generating heart rate and blood pressure oscillations in phase with respiration. Our data reveal yet more functions entrained to the activity of the preB{\"o}tC, with a role in generating cardiorespiratory oscillations. The findings have implications for cardiovascular pathologies, such as hypertension and heart failure, where respiratory entrainment of heart rate is diminished and respiratory entrainment of blood pressure exaggerated.",

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author = "Cl{\'e}ment Menuet and Connelly, {Angela A.} and Bassi, {Jaspreet K.} and Melo, {Mariana R.} and Sheng Le and Jessica Kamar and Kumar, {Natasha N.} and McDougall, {Stuart J.} and Simon McMullan and Allen, {Andrew M.}",

note = "Copyright the Author(s). Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.",

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doi = "10.7554/eLife.57288",

language = "English",

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AU - Menuet, Clément

AU - Connelly, Angela A.

AU - Bassi, Jaspreet K.

AU - Melo, Mariana R.

AU - Le, Sheng

AU - Kamar, Jessica

AU - Kumar, Natasha N.

AU - McDougall, Stuart J.

AU - McMullan, Simon

AU - Allen, Andrew M.

N1 - Copyright the Author(s). Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

PY - 2020/6/15

Y1 - 2020/6/15

N2 - Heart rate and blood pressure oscillate in phase with respiratory activity. A component of these oscillations is generated centrally, with respiratory neurons entraining the activity of pre-sympathetic and parasympathetic cardiovascular neurons. Using a combination of optogenetic inhibition and excitation in vivo and in situ in rats, as well as neuronal tracing, we demonstrate that preBötzinger Complex (preBötC) neurons, which form the kernel for inspiratory rhythm generation, directly modulate cardiovascular activity. Specifically, inhibitory preBötC neurons modulate cardiac parasympathetic neuron activity whilst excitatory preBötC neurons modulate sympathetic vasomotor neuron activity, generating heart rate and blood pressure oscillations in phase with respiration. Our data reveal yet more functions entrained to the activity of the preBötC, with a role in generating cardiorespiratory oscillations. The findings have implications for cardiovascular pathologies, such as hypertension and heart failure, where respiratory entrainment of heart rate is diminished and respiratory entrainment of blood pressure exaggerated.

AB - Heart rate and blood pressure oscillate in phase with respiratory activity. A component of these oscillations is generated centrally, with respiratory neurons entraining the activity of pre-sympathetic and parasympathetic cardiovascular neurons. Using a combination of optogenetic inhibition and excitation in vivo and in situ in rats, as well as neuronal tracing, we demonstrate that preBötzinger Complex (preBötC) neurons, which form the kernel for inspiratory rhythm generation, directly modulate cardiovascular activity. Specifically, inhibitory preBötC neurons modulate cardiac parasympathetic neuron activity whilst excitatory preBötC neurons modulate sympathetic vasomotor neuron activity, generating heart rate and blood pressure oscillations in phase with respiration. Our data reveal yet more functions entrained to the activity of the preBötC, with a role in generating cardiorespiratory oscillations. The findings have implications for cardiovascular pathologies, such as hypertension and heart failure, where respiratory entrainment of heart rate is diminished and respiratory entrainment of blood pressure exaggerated.

KW - cardiorespiratory control

KW - master oscillator

KW - neuroscience

KW - optogenetic inhibition

KW - prebötzinger complex

KW - rat

KW - respiratory sinus arrhythmia

KW - respiratory-sympathetic modulation

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PreBötzinger complex neurons drive respiratory modulation of blood pressure and heart rate

Abstract

Bibliographical note

Keywords

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Mapping the connectome that controls blood pressure

Cite this

PreBötzinger complex neurons drive respiratory modulation of blood pressure and heart rate

Abstract

Bibliographical note

Keywords

Access to Document

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Fingerprint

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Mapping the connectome that controls blood pressure

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