The cerebral cost of breathing: an FMRI case-study in congenital central hypoventilation syndrome.
PLoS One. 2014; 9(9):e107850.Plos

Abstract

Certain motor activities--like walking or breathing--present the interesting property of proceeding either automatically or under voluntary control. In the case of breathing, brainstem structures located in the medulla are in charge of the automatic mode, whereas cortico-subcortical brain networks--including various frontal lobe areas--subtend the voluntary mode. We speculated that the involvement of cortical activity during voluntary breathing could impact both on the "resting state" pattern of cortical-subcortical connectivity, and on the recruitment of executive functions mediated by the frontal lobe. In order to test this prediction we explored a patient suffering from central congenital hypoventilation syndrome (CCHS), a very rare developmental condition secondary to brainstem dysfunction. Typically, CCHS patients demonstrate efficient cortically-controlled breathing while awake, but require mechanically-assisted ventilation during sleep to overcome the inability of brainstem structures to mediate automatic breathing. We used simultaneous EEG-fMRI recordings to compare patterns of brain activity between these two types of ventilation during wakefulness. As compared with spontaneous breathing (SB), mechanical ventilation (MV) restored the default mode network (DMN) associated with self-consciousness, mind-wandering, creativity and introspection in healthy subjects. SB on the other hand resulted in a specific increase of functional connectivity between brainstem and frontal lobe. Behaviorally, the patient was more efficient in cognitive tasks requiring executive control during MV than during SB, in agreement with her subjective reports in everyday life. Taken together our results provide insight into the cognitive and neural costs of spontaneous breathing in one CCHS patient, and suggest that MV during waking periods may free up frontal lobe resources, and make them available for cognitive recruitment. More generally, this study reveals how the active maintenance of cortical control over a continuous motor activity impacts on brain functioning and cognition.

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Authors+Show Affiliations

Sharman M

Gallea C

Institut National de la Santé et de la Recherche Médicale (INSERM), Institut du Cerveau et de la Moelle Epinière (ICM), Unité Mixte de Recherche 1127, (CENIR), Paris, France.

Lehongre K

Galanaud D

Institut National de la Santé et de la Recherche Médicale (INSERM), Institut du Cerveau et de la Moelle Epinière (ICM), Unité Mixte de Recherche 1127, (CENIR), Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié- Salpêtrière Charles Foix, Department of Neuroradiology, Paris, France; Université Pierre et Marie Curie-Paris 6, Faculté de Médecine Pitié-Salpêtrière, Paris, France.

Nicolas N

Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié- Salpêtrière Charles Foix, Centre d'Investigation Clinique 1421, Paris, France.

Similowski T

Cohen L

Institut National de la Santé et de la Recherche Médicale (INSERM), Institut du Cerveau et de la Moelle Epinière (ICM), Unité Mixte de Recherche 1127, PICNIC Lab, Paris, France; Centre National de la Recherche Scientifique (CNRS), Institut du Cerveau et de la Moelle Epinière (ICM), Unité 7225, PICNIC Lab, Paris, France; Université Pierre et Marie Curie-Paris 6, Faculté de Médecine Pitié-Salpêtrière, Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié-Salpêtrière Charles Foix, Department of Neurology, Paris, France.

Straus C

Université Pierre et Marie Curie-Paris 6, Faculté de Médecine Pitié-Salpêtrière, Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service de Pneumologie et Réanimation Médicale (Département "R3S"), Paris, France; Sorbonne Universités, Université Pierre et Marie Curie-Paris 6, Unité Mixte de Recherche 1158 "Neurophysiologie Respiratoire Expérimentale et Clinique", Paris, France; Institut National de la Santé et de la Recherche Médicale (INSERM), Unité Mixte de Recherche 1158 "Neurophysiologie Respiratoire Expérimentale et Clinique", Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Service des Explorations Fonctionnelles de la Respiration, de l'Exercice et de la Dyspnée (Département "R3S"), Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe Hospitalier Pitié-Salpêtrière Charles Foix, Centre de Référence Maladies Rares "syndrome d'Ondine", Paris, France.

Naccache L

Institut National de la Santé et de la Recherche Médicale (INSERM), Institut du Cerveau et de la Moelle Epinière (ICM), Unité Mixte de Recherche 1127, PICNIC Lab, Paris, France; Centre National de la Recherche Scientifique (CNRS), Institut du Cerveau et de la Moelle Epinière (ICM), Unité 7225, PICNIC Lab, Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié- Salpêtrière Charles Foix, Centre d'Investigation Clinique 1421, Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié-Salpêtrière Charles Foix, Department of Neurology, Paris, France; Assistance Publique-Hôpitaux de Paris, Groupe hospitalier Pitié-Salpêtrière Charles Foix, Department of Neurophysiology, Paris, France.

MeSH

AdultAwarenessBrain MappingCaudate NucleusExecutive FunctionFemaleFrontal LobeGyrus CinguliHumansHypoventilationMagnetic Resonance ImagingRespirationRespiration, ArtificialSleep Apnea, Central

Pub Type(s)

Journal Article

Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

25268234

Clinical Trial Links

Clinical trial which this article describes

Citation

Sharman, Mike, et al. "The Cerebral Cost of Breathing: an FMRI Case-study in Congenital Central Hypoventilation Syndrome." PloS One, vol. 9, no. 9, 2014, pp. e107850.

Sharman M, Gallea C, Lehongre K, et al. The cerebral cost of breathing: an FMRI case-study in congenital central hypoventilation syndrome. PLoS One. 2014;9(9):e107850.

Sharman, M., Gallea, C., Lehongre, K., Galanaud, D., Nicolas, N., Similowski, T., Cohen, L., Straus, C., & Naccache, L. (2014). The cerebral cost of breathing: an FMRI case-study in congenital central hypoventilation syndrome. PloS One, 9(9), e107850. https://doi.org/10.1371/journal.pone.0107850

Sharman M, et al. The Cerebral Cost of Breathing: an FMRI Case-study in Congenital Central Hypoventilation Syndrome. PLoS One. 2014;9(9):e107850. PubMed PMID: 25268234.

* Article titles in AMA citation format should be in sentence-case

TY - JOUR T1 - The cerebral cost of breathing: an FMRI case-study in congenital central hypoventilation syndrome. AU - Sharman,Mike, AU - Gallea,Cécile, AU - Lehongre,Katia, AU - Galanaud,Damien, AU - Nicolas,Nathalie, AU - Similowski,Thomas, AU - Cohen,Laurent, AU - Straus,Christian, AU - Naccache,Lionel, Y1 - 2014/09/30/ PY - 2014/03/17/received PY - 2014/08/16/accepted PY - 2014/10/1/entrez PY - 2014/10/1/pubmed PY - 2015/6/26/medline SP - e107850 EP - e107850 JF - PloS one JO - PLoS One VL - 9 IS - 9 N2 - Certain motor activities--like walking or breathing--present the interesting property of proceeding either automatically or under voluntary control. In the case of breathing, brainstem structures located in the medulla are in charge of the automatic mode, whereas cortico-subcortical brain networks--including various frontal lobe areas--subtend the voluntary mode. We speculated that the involvement of cortical activity during voluntary breathing could impact both on the "resting state" pattern of cortical-subcortical connectivity, and on the recruitment of executive functions mediated by the frontal lobe. In order to test this prediction we explored a patient suffering from central congenital hypoventilation syndrome (CCHS), a very rare developmental condition secondary to brainstem dysfunction. Typically, CCHS patients demonstrate efficient cortically-controlled breathing while awake, but require mechanically-assisted ventilation during sleep to overcome the inability of brainstem structures to mediate automatic breathing. We used simultaneous EEG-fMRI recordings to compare patterns of brain activity between these two types of ventilation during wakefulness. As compared with spontaneous breathing (SB), mechanical ventilation (MV) restored the default mode network (DMN) associated with self-consciousness, mind-wandering, creativity and introspection in healthy subjects. SB on the other hand resulted in a specific increase of functional connectivity between brainstem and frontal lobe. Behaviorally, the patient was more efficient in cognitive tasks requiring executive control during MV than during SB, in agreement with her subjective reports in everyday life. Taken together our results provide insight into the cognitive and neural costs of spontaneous breathing in one CCHS patient, and suggest that MV during waking periods may free up frontal lobe resources, and make them available for cognitive recruitment. More generally, this study reveals how the active maintenance of cortical control over a continuous motor activity impacts on brain functioning and cognition. SN - 1932-6203 UR - https://www.unboundmedicine.com/medline/citation/25268234/The_cerebral_cost_of_breathing:_an_FMRI_case_study_in_congenital_central_hypoventilation_syndrome_ DB - PRIME DP - Unbound Medicine ER -

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The cerebral cost of breathing: an FMRI case-study in congenital central hypoventilation syndrome.PLoS One. 2014; 9(9):e107850.Plos