Normobaric Hyperoxia (95% O2) Stimulates CO2-Sensitive and CO2-Insensitive Neurons in the Caudal Solitary Complex of Rat Medullary Tissue Slices Maintained in 40% O2

Michael P. Matott; G. E. Ciarlone; Robert W. Putnam; J. B. Dean

doi:10.1016/j.neuroscience.2014.03.017

Normobaric Hyperoxia (95% O₂) Stimulates CO₂-Sensitive and CO₂-Insensitive Neurons in the Caudal Solitary Complex of Rat Medullary Tissue Slices Maintained in 40% O₂

Michael P. Matott, G. E. Ciarlone, Robert W. Putnam, J. B. Dean

Wright State University

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

Abstract

We tested the hypothesis that decreasing the control level of O ₂ from 95% to 40% reduces tissue partial pressure of oxygen (pO ₂ ), decreases extracellular nitric oxide ( NO) and decreases intracellular superoxide ( O ₂ ⁻ ) while maintaining viability in caudal solitary complex (cSC) neurons in slices (∼300–400 μm; neonatal rat P2–22; 34–37 °C). We also tested the hypothesis that normobaric hyperoxia is a general stimulant of cSC neurons, including CO ₂ -excited neurons. Whole-cell recordings of cSC neurons maintained in 40% O ₂ were comparable to recordings made in 95% O ₂ in duration and quality. In 40% O ₂ , cSC neurons had a significantly lower spontaneous firing rate but similar membrane potentials and input resistances as cSC neurons maintained in 95% O ₂ . Tissue pO ₂ was threefold lower in 40% O ₂ versus 95% O ₂ . Likewise, extracellular NO and intracellular O ₂ ⁻ were lower in 40% versus 95% O ₂ . 67% of neurons maintained in 40% O ₂ control were stimulated by hyperoxia (95% O ₂ ) compared to 81% of neurons maintained in 95% O ₂ that were stimulated during hyperoxic reoxygenation following acute exposure to 0–40% O ₂ . cSC slices maintained in 40% O ₂ exhibited CO ₂ -chemosensitive neurons, including CO ₂ -excited (31.5%) and a higher incidence of CO ₂ -inhibited (31.5%) neurons than previously reported. Likewise, a higher incidence of CO ₂ -inhibited and lower incidence of CO ₂ -excited neurons were observed in 85–95% O ₂ . 82% of O ₂ -excited neurons were also CO ₂ -chemosensitive; CO ₂ -excited (86%) and CO ₂ -inhibited neurons (84%) were equally stimulated by hyperoxia. Our findings demonstrate that chronic (hours) and acute (minutes) exposure to hyperoxia stimulates firing rate in the majority of cSC neurons, most of which are also CO ₂ chemosensitive. Our findings support the hypothesis that recurring exposures to acute hyperoxia and hyperoxic reoxygenation—a repeating surge in tissue pO ₂ —activate redox and nitrosative signaling mechanisms in CO ₂ -chemosensitive neurons that alter expression of CO ₂ chemosensitivity (e.g., increased expression of CO ₂ -inhibition) compared to sustained hyperoxia (85–95% O ₂ ).

Original language	American English
Journal	Neuroscience
Volume	270
DOIs	https://doi.org/10.1016/j.neuroscience.2014.03.017
State	Published - Jun 13 2014

Disciplines

Medical Cell Biology
Medical Neurobiology
Medical Physiology
Medical Sciences
Medicine and Health Sciences
Neurosciences
Physiological Processes

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@article{47d8dbc321dc4fedb7e96049183fb005,

title = "Normobaric Hyperoxia (95% O2) Stimulates CO2-Sensitive and CO2-Insensitive Neurons in the Caudal Solitary Complex of Rat Medullary Tissue Slices Maintained in 40% O2",

abstract = " We tested the hypothesis that decreasing the control level of O 2 from 95% to 40% reduces tissue partial pressure of oxygen (pO 2 ), decreases extracellular nitric oxide ( NO) and decreases intracellular superoxide ( O 2 − ) while maintaining viability in caudal solitary complex (cSC) neurons in slices (∼300–400 μm; neonatal rat P2–22; 34–37 °C). We also tested the hypothesis that normobaric hyperoxia is a general stimulant of cSC neurons, including CO 2 -excited neurons. Whole-cell recordings of cSC neurons maintained in 40% O 2 were comparable to recordings made in 95% O 2 in duration and quality. In 40% O 2 , cSC neurons had a significantly lower spontaneous firing rate but similar membrane potentials and input resistances as cSC neurons maintained in 95% O 2 . Tissue pO 2 was threefold lower in 40% O 2 versus 95% O 2 . Likewise, extracellular NO and intracellular O 2 − were lower in 40% versus 95% O 2 . 67% of neurons maintained in 40% O 2 control were stimulated by hyperoxia (95% O 2 ) compared to 81% of neurons maintained in 95% O 2 that were stimulated during hyperoxic reoxygenation following acute exposure to 0–40% O 2 . cSC slices maintained in 40% O 2 exhibited CO 2 -chemosensitive neurons, including CO 2 -excited (31.5%) and a higher incidence of CO 2 -inhibited (31.5%) neurons than previously reported. Likewise, a higher incidence of CO 2 -inhibited and lower incidence of CO 2 -excited neurons were observed in 85–95% O 2 . 82% of O 2 -excited neurons were also CO 2 -chemosensitive; CO 2 -excited (86%) and CO 2 -inhibited neurons (84%) were equally stimulated by hyperoxia. Our findings demonstrate that chronic (hours) and acute (minutes) exposure to hyperoxia stimulates firing rate in the majority of cSC neurons, most of which are also CO 2 chemosensitive. Our findings support the hypothesis that recurring exposures to acute hyperoxia and hyperoxic reoxygenation—a repeating surge in tissue pO 2 —activate redox and nitrosative signaling mechanisms in CO 2 -chemosensitive neurons that alter expression of CO 2 chemosensitivity (e.g., increased expression of CO 2 -inhibition) compared to sustained hyperoxia (85–95% O 2 ).",

author = "Matott, {Michael P.} and Ciarlone, {G. E.} and Putnam, {Robert W.} and Dean, {J. B.}",

year = "2014",

month = jun,

day = "13",

doi = "10.1016/j.neuroscience.2014.03.017",

language = "American English",

volume = "270",

journal = "Neuroscience",

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TY - JOUR

T1 - Normobaric Hyperoxia (95% O2) Stimulates CO2-Sensitive and CO2-Insensitive Neurons in the Caudal Solitary Complex of Rat Medullary Tissue Slices Maintained in 40% O2

AU - Matott, Michael P.

AU - Ciarlone, G. E.

AU - Putnam, Robert W.

AU - Dean, J. B.

PY - 2014/6/13

Y1 - 2014/6/13

N2 - We tested the hypothesis that decreasing the control level of O 2 from 95% to 40% reduces tissue partial pressure of oxygen (pO 2 ), decreases extracellular nitric oxide ( NO) and decreases intracellular superoxide ( O 2 − ) while maintaining viability in caudal solitary complex (cSC) neurons in slices (∼300–400 μm; neonatal rat P2–22; 34–37 °C). We also tested the hypothesis that normobaric hyperoxia is a general stimulant of cSC neurons, including CO 2 -excited neurons. Whole-cell recordings of cSC neurons maintained in 40% O 2 were comparable to recordings made in 95% O 2 in duration and quality. In 40% O 2 , cSC neurons had a significantly lower spontaneous firing rate but similar membrane potentials and input resistances as cSC neurons maintained in 95% O 2 . Tissue pO 2 was threefold lower in 40% O 2 versus 95% O 2 . Likewise, extracellular NO and intracellular O 2 − were lower in 40% versus 95% O 2 . 67% of neurons maintained in 40% O 2 control were stimulated by hyperoxia (95% O 2 ) compared to 81% of neurons maintained in 95% O 2 that were stimulated during hyperoxic reoxygenation following acute exposure to 0–40% O 2 . cSC slices maintained in 40% O 2 exhibited CO 2 -chemosensitive neurons, including CO 2 -excited (31.5%) and a higher incidence of CO 2 -inhibited (31.5%) neurons than previously reported. Likewise, a higher incidence of CO 2 -inhibited and lower incidence of CO 2 -excited neurons were observed in 85–95% O 2 . 82% of O 2 -excited neurons were also CO 2 -chemosensitive; CO 2 -excited (86%) and CO 2 -inhibited neurons (84%) were equally stimulated by hyperoxia. Our findings demonstrate that chronic (hours) and acute (minutes) exposure to hyperoxia stimulates firing rate in the majority of cSC neurons, most of which are also CO 2 chemosensitive. Our findings support the hypothesis that recurring exposures to acute hyperoxia and hyperoxic reoxygenation—a repeating surge in tissue pO 2 —activate redox and nitrosative signaling mechanisms in CO 2 -chemosensitive neurons that alter expression of CO 2 chemosensitivity (e.g., increased expression of CO 2 -inhibition) compared to sustained hyperoxia (85–95% O 2 ).

AB - We tested the hypothesis that decreasing the control level of O 2 from 95% to 40% reduces tissue partial pressure of oxygen (pO 2 ), decreases extracellular nitric oxide ( NO) and decreases intracellular superoxide ( O 2 − ) while maintaining viability in caudal solitary complex (cSC) neurons in slices (∼300–400 μm; neonatal rat P2–22; 34–37 °C). We also tested the hypothesis that normobaric hyperoxia is a general stimulant of cSC neurons, including CO 2 -excited neurons. Whole-cell recordings of cSC neurons maintained in 40% O 2 were comparable to recordings made in 95% O 2 in duration and quality. In 40% O 2 , cSC neurons had a significantly lower spontaneous firing rate but similar membrane potentials and input resistances as cSC neurons maintained in 95% O 2 . Tissue pO 2 was threefold lower in 40% O 2 versus 95% O 2 . Likewise, extracellular NO and intracellular O 2 − were lower in 40% versus 95% O 2 . 67% of neurons maintained in 40% O 2 control were stimulated by hyperoxia (95% O 2 ) compared to 81% of neurons maintained in 95% O 2 that were stimulated during hyperoxic reoxygenation following acute exposure to 0–40% O 2 . cSC slices maintained in 40% O 2 exhibited CO 2 -chemosensitive neurons, including CO 2 -excited (31.5%) and a higher incidence of CO 2 -inhibited (31.5%) neurons than previously reported. Likewise, a higher incidence of CO 2 -inhibited and lower incidence of CO 2 -excited neurons were observed in 85–95% O 2 . 82% of O 2 -excited neurons were also CO 2 -chemosensitive; CO 2 -excited (86%) and CO 2 -inhibited neurons (84%) were equally stimulated by hyperoxia. Our findings demonstrate that chronic (hours) and acute (minutes) exposure to hyperoxia stimulates firing rate in the majority of cSC neurons, most of which are also CO 2 chemosensitive. Our findings support the hypothesis that recurring exposures to acute hyperoxia and hyperoxic reoxygenation—a repeating surge in tissue pO 2 —activate redox and nitrosative signaling mechanisms in CO 2 -chemosensitive neurons that alter expression of CO 2 chemosensitivity (e.g., increased expression of CO 2 -inhibition) compared to sustained hyperoxia (85–95% O 2 ).

UR - https://corescholar.libraries.wright.edu/ncbp/1111

U2 - 10.1016/j.neuroscience.2014.03.017

DO - 10.1016/j.neuroscience.2014.03.017

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JO - Neuroscience

JF - Neuroscience

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