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Articles, Systems/Circuits

Neurophysiological Evidence for a Cortical Contribution to the Wakefulness-Related Drive to Breathe Explaining Hypocapnia-Resistant Ventilation in Humans

Matthieu Dubois, Cécile Chenivesse, Mathieu Raux, Adrian Morales-Robles, Marie-Cécile Nierat, Gilles Garcia, Xavier Navarro-Sune, Mario Chavez, Jacques Martinerie and Thomas Similowski
Journal of Neuroscience 12 October 2016, 36 (41) 10673-10682; DOI: https://doi.org/10.1523/JNEUROSCI.2376-16.2016
Matthieu Dubois
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
2Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service de Pneumologie et Réanimation Médicale Département R3S, F-75013 Paris, France,
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Cécile Chenivesse
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
2Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service de Pneumologie et Réanimation Médicale Département R3S, F-75013 Paris, France,
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Mathieu Raux
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
3Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Département d'Anesthésie-Réanimation, F-75013 Paris, France, and
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Adrian Morales-Robles
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
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Marie-Cécile Nierat
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
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Gilles Garcia
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
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Xavier Navarro-Sune
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
4Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225, Institut du Cerveau et de la Moëlle, F-75013 Paris, France
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Mario Chavez
4Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225, Institut du Cerveau et de la Moëlle, F-75013 Paris, France
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Jacques Martinerie
4Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7225, Institut du Cerveau et de la Moëlle, F-75013 Paris, France
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Thomas Similowski
1Sorbonne Université, Université Paris 06 Pierre et Marie Curie and Institut National de la Santé et de la Rercherche Médicale, Unité Mixte de Recherche-Santé 1158 Neurophysiologie Respiratoire Expérimentale et Clinique, F-75013 Paris, France,
2Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service de Pneumologie et Réanimation Médicale Département R3S, F-75013 Paris, France,
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Abstract

Spontaneous ventilation in mammals is driven by automatic brainstem networks that generate the respiratory rhythm and increase ventilation in the presence of increased carbon dioxide production. Hypocapnia decreases the drive to breathe and induces apnea. In humans, this occurs during sleep but not during wakefulness. We hypothesized that hypocapnic breathing would be associated with respiratory-related cortical activity similar to that observed during volitional breathing, inspiratory constraints, or in patients with defective automatic breathing (preinspiratory potentials). Nineteen healthy subjects were studied under passive (mechanical ventilation, n = 10) or active (voluntary hyperventilation, n = 9) profound hypocapnia. Ventilatory and electroencephalographic recordings were performed during voluntary sniff maneuvers, normocapnic breathing, hypocapnia, and after return to normocapnia. EEG recordings were analyzed with respect to the ventilatory flow signal to detect preinspiratory potentials in frontocentral electrodes and to construct time-frequency maps. After passive hyperventilation, hypocapnia was associated with apnea in 3 cases and ventilation persisted in 7 cases (3 and 6 after active hyperventilation, respectively). No respiratory-related EEG activity was observed in subjects with hypocapnia-related apneas. In contrast, preinspiratory potentials were present at vertex recording sites in 12 of the remaining 13 subjects (p < 0.001). This was corroborated by time-frequency maps. This study provides direct evidence of a cortical substrate to hypocapnic breathing in awake humans and fuels the notion of corticosubcortical cooperation to preserve human ventilation in a variety of situations. Of note, maintaining ventilatory activity at low carbon dioxide levels is among the prerequisites to speech production insofar as speech often induces hypocapnia.

SIGNIFICANCE STATEMENT Human ventilatory activity persists, during wakefulness, even when hypocapnia makes it unnecessary. This peculiarity of human breathing control is important to speech and speech-breathing insofar as speech induces hypocapnia. This study evidences a specific respiratory-related cortical activity. This suggests that human hypocapnic breathing is driven, at least in part, by cortical mechanisms similar to those involved in volitional breathing, in breathing against mechanical constraints or with weak inspiratory muscle, and in patients with defective medullary breathing pattern generators. This fuels the notion that the human ventilatory drive during wakefulness often results from a corticosubcortical cooperation, and opens new avenues to study certain ventilatory and speech disorders.

  • cerebral cortex
  • control of breathing
  • hypocapnia
  • respiration
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The Journal of Neuroscience: 36 (41)
Journal of Neuroscience
Vol. 36, Issue 41
12 Oct 2016
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Neurophysiological Evidence for a Cortical Contribution to the Wakefulness-Related Drive to Breathe Explaining Hypocapnia-Resistant Ventilation in Humans
Matthieu Dubois, Cécile Chenivesse, Mathieu Raux, Adrian Morales-Robles, Marie-Cécile Nierat, Gilles Garcia, Xavier Navarro-Sune, Mario Chavez, Jacques Martinerie, Thomas Similowski
Journal of Neuroscience 12 October 2016, 36 (41) 10673-10682; DOI: 10.1523/JNEUROSCI.2376-16.2016

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Neurophysiological Evidence for a Cortical Contribution to the Wakefulness-Related Drive to Breathe Explaining Hypocapnia-Resistant Ventilation in Humans
Matthieu Dubois, Cécile Chenivesse, Mathieu Raux, Adrian Morales-Robles, Marie-Cécile Nierat, Gilles Garcia, Xavier Navarro-Sune, Mario Chavez, Jacques Martinerie, Thomas Similowski
Journal of Neuroscience 12 October 2016, 36 (41) 10673-10682; DOI: 10.1523/JNEUROSCI.2376-16.2016
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Keywords

  • cerebral cortex
  • control of breathing
  • hypocapnia
  • respiration

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