Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants

We mapped and characterized changes in the activity of brainstem cell groups under hypoxia in one-day-old newborn mice, an animal model in which the central nervous system at birth is particularly immature. The classical biphasic respiratory response characterized by transient hyperventilation, foll...

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Main Authors: Fanny JOUBERT, Camille LOISEAU, Anne-Sophie PERRIN-TERRIN, Florence CAYETANOT, Alain FRUGIERE, Nicolas Voituron, Laurence Bodineau
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-12-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00609/full
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author Fanny JOUBERT
Camille LOISEAU
Anne-Sophie PERRIN-TERRIN
Anne-Sophie PERRIN-TERRIN
Florence CAYETANOT
Alain FRUGIERE
Nicolas Voituron
Laurence Bodineau
author_facet Fanny JOUBERT
Camille LOISEAU
Anne-Sophie PERRIN-TERRIN
Anne-Sophie PERRIN-TERRIN
Florence CAYETANOT
Alain FRUGIERE
Nicolas Voituron
Laurence Bodineau
author_sort Fanny JOUBERT
collection DOAJ
description We mapped and characterized changes in the activity of brainstem cell groups under hypoxia in one-day-old newborn mice, an animal model in which the central nervous system at birth is particularly immature. The classical biphasic respiratory response characterized by transient hyperventilation, followed by severe ventilation decline, was associated with increased c-FOS immunoreactivity in brainstem cell groups: the nucleus of the solitary tract, ventral reticular nucleus of the medulla, retrotrapezoid/parafacial region, parapyramidal group, raphe magnus nucleus, lateral and medial parabrachial nucleus, and dorsal subcoeruleus nucleus. In contrast, the hypoglossal nucleus displayed decreased c-FOS immunoreactivity. There were fewer or no activated catecholaminergic cells activated in the medulla oblongata, whereas approximately 45% of the c-FOS-positive cells in the dorsal subcoeruleus were co-labelled. Approximately 30% of the c-FOS-positive cells in the parapyramidal group were serotoninergic, whereas only a small portion were labelled for serotonin in the raphe magnus nucleus. None of the c-FOS-positive cells in the retrotrapezoid/parafacial region were co-labelled for PHOX2B. Thus, the hypoxia-activated brainstem neuronal network of one-day-old mice is characterized by i) the activation of catecholaminergic cells of the dorsal subcoeruleus nucleus, a structure implicated in the strong depressive pontine influence previously reported in the fetus but not in newborns, ii) the weak activation of catecholaminergic cells of the ventral reticular nucleus of the medulla, an area involved in hypoxic hyperventilation, and iii) the absence of PHOX2B-positive cells activated in the retrotrapezoid/parafacial region. Based on these results, one-day-old mice could highlight characteristics for modelling the breathing network of premature infants.
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spelling doaj.art-648ae56d465c45e49bb1c964335391db2022-12-22T01:43:01ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2016-12-01710.3389/fphys.2016.00609216075Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infantsFanny JOUBERT0Camille LOISEAU1Anne-Sophie PERRIN-TERRIN2Anne-Sophie PERRIN-TERRIN3Florence CAYETANOT4Alain FRUGIERE5Nicolas Voituron6Laurence Bodineau7UMR_S1158 - Inserm/UPMCUMR_S1158 - Inserm/UPMCUMR_S1158 - Inserm/UPMCEA2363 Université de BobignyCNRS, UMR 7289 - Aix Marseille UniversitéUMR_S1158 - Inserm/UPMCEA2363 Université de BobignyUMR_S1158 - Inserm/UPMCWe mapped and characterized changes in the activity of brainstem cell groups under hypoxia in one-day-old newborn mice, an animal model in which the central nervous system at birth is particularly immature. The classical biphasic respiratory response characterized by transient hyperventilation, followed by severe ventilation decline, was associated with increased c-FOS immunoreactivity in brainstem cell groups: the nucleus of the solitary tract, ventral reticular nucleus of the medulla, retrotrapezoid/parafacial region, parapyramidal group, raphe magnus nucleus, lateral and medial parabrachial nucleus, and dorsal subcoeruleus nucleus. In contrast, the hypoglossal nucleus displayed decreased c-FOS immunoreactivity. There were fewer or no activated catecholaminergic cells activated in the medulla oblongata, whereas approximately 45% of the c-FOS-positive cells in the dorsal subcoeruleus were co-labelled. Approximately 30% of the c-FOS-positive cells in the parapyramidal group were serotoninergic, whereas only a small portion were labelled for serotonin in the raphe magnus nucleus. None of the c-FOS-positive cells in the retrotrapezoid/parafacial region were co-labelled for PHOX2B. Thus, the hypoxia-activated brainstem neuronal network of one-day-old mice is characterized by i) the activation of catecholaminergic cells of the dorsal subcoeruleus nucleus, a structure implicated in the strong depressive pontine influence previously reported in the fetus but not in newborns, ii) the weak activation of catecholaminergic cells of the ventral reticular nucleus of the medulla, an area involved in hypoxic hyperventilation, and iii) the absence of PHOX2B-positive cells activated in the retrotrapezoid/parafacial region. Based on these results, one-day-old mice could highlight characteristics for modelling the breathing network of premature infants.http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00609/fullSerotoninc-foscatecholamineSubcoeruleus nucleusPHOX2BHypoxic ventilatory depression
spellingShingle Fanny JOUBERT
Camille LOISEAU
Anne-Sophie PERRIN-TERRIN
Anne-Sophie PERRIN-TERRIN
Florence CAYETANOT
Alain FRUGIERE
Nicolas Voituron
Laurence Bodineau
Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
Frontiers in Physiology
Serotonin
c-fos
catecholamine
Subcoeruleus nucleus
PHOX2B
Hypoxic ventilatory depression
title Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
title_full Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
title_fullStr Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
title_full_unstemmed Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
title_short Key brainstem structures activated during hypoxic exposure in one-day-old mice highlight characteristics for modelling breathing network in premature infants
title_sort key brainstem structures activated during hypoxic exposure in one day old mice highlight characteristics for modelling breathing network in premature infants
topic Serotonin
c-fos
catecholamine
Subcoeruleus nucleus
PHOX2B
Hypoxic ventilatory depression
url http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00609/full
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