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European Journal of Applied Physiology
Published in: European Journal of Applied Physiology 3/2024

17-12-2023 | Dyspnea | Invited Review

Breath-holding as model for the evaluation of EEG signal during respiratory distress

Authors: Lucas de Jesus Alves Ribeiro, Victor Hugo do Vale Bastos, Marcelo Coertjens

Published in: European Journal of Applied Physiology | Issue 3/2024

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Abstract

Purpose

Research describes the existence of a relationship between cortical activity and the regulation of bulbar respiratory centers through the evaluation of the electroencephalographic (EEG) signal during respiratory challenges. For example, we found evidences of a reduction in the frequency of the EEG (alpha band) in both divers and non-divers during apnea tests. For instance, this reduction was more prominent in divers due to the greater physiological disturbance resulting from longer apnea time. However, little is known about EEG adaptations during tests of maximal apnea, a test that voluntarily stops breathing and induces dyspnea.

Results

Through this mini-review, we verified that a protocol of successive apneas triggers a significant increase in the maximum apnea time and we hypothesized that successive maximal apnea test could be a powerful model for the study of cortical activity during respiratory distress.

Conclusion

Dyspnea is a multifactorial symptom and we believe that performing a successive maximal apnea protocol is possible to understand some factors that determine the sensation of dyspnea through the EEG signal, especially in people not trained in apnea.
Literature
Agostoni E (1963) Diaphragm activity during breath holding: factors related to its onset. J Appl Physiol 18:30–36PubMedCrossRef
Andersson J, Schagatay E (1998) Effects of lung volume and involuntary breathing movements on the human diving response. Eur J Appl Physiol Occup Physiol 77(1–2):19–24PubMed
Ando S, Komiyama T, Sudo M, Higaki Y, Ishida K, Costello JT, Katayama K (2020) The interactive effects of acute exercise and hypoxia on cognitive performance: a narrative review. Scand J Med Sci Sports 30(3):384–398PubMedCrossRef
Arce-Álvarez A, Veliz C, Vazquez-Muñoz M, von Igel M, Alvares C, Ramirez-Campillo R, Izquierdo M, Millet GP, Del Rio R, Andrade DC (2021) Hypoxic respiratory chemoreflex control in young trained swimmers. Front Physiol 26(12):632603CrossRef
Bain AR, Drvis I, Dujic Z, MacLeod DB, Ainslie PN (2018) Physiology of static breath holding in elite apneists. Exp Physiol 103(5):635–651PubMedCrossRef
Baković D, Valic Z, Eterović D, Vukovic I, Obad A, Marinović-Terzić I, Dujić Z (2003) Spleen volume and blood flow response to repeated breath-hold apneas. J Appl Physiol 95(4):1460–1466PubMedCrossRef
Bartlett DJ (1977) Effects of Valsalva and Mueller maneuvers on breath-holding time. J Appl Physiol Respir Environ Exerc Physiol 42(5):717–721PubMed
Benarroch EE (1993) The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc 68(10):988–1001PubMedCrossRef
Berger BG, Owen DR (1988) Stress reduction and mood enhancement in four exercise modes: swimming, body conditioning, Hatha yoga, and fencing. Res Quart Exer Sport 59(2):148–159CrossRef
Bordoni B, Zanier E (2013) Anatomic connections of the diaphragm: influence of respiration on the body system. J Multidiscip Healthc 25(6):281–291CrossRef
Cross TJ, Breskovic T, Sabapathy S, Zubin Maslov P, Johnson BD, Dujic Z (2013) Respiratory muscle pressure development during breath holding in apnea divers. Med Sci Sports Exerc 45(1):93–101PubMedCrossRef
Delapille P, Verin E, Tourny-Chollet C, Pasquis P (2001) Breath-holding time: effects of non-chemical factors in divers and non-divers. Pflugers Arch 442(4):588–594PubMedCrossRef
Dimitriadis SI, Brindley L, Evans LH, Linden DE, Singh KD (2018) A novel, fast, reliable, and data-driven method for simultaneous single-trial mining and amplitude-latency estimation based on proximity graphs and network analysis. Front Neuroinform 19(12):59CrossRef
Diniz CM, Farias TL, Pereira MC, Pires CB, Gonçalves LS, Coertjens PC, Coertjens M (2014) Chronic adaptations of lung function in breath-hold diving fishermen. Int J Occup Med Environ Health 27(2):216–223PubMedCrossRef
Elia A, Gennser M, Harlow PS, Lees MJ (2021) Physiology, pathophysiology and (mal)adaptations to chronic apnoeic training: a state-of-the-art review. Eur J Appl Physiol 121(6):1543–1566PubMedPubMedCentralCrossRef
Espersen K, Frandsen H, Lorentzen T, Kanstrup IL, Christensen NJ (2002) The human spleen as an erythrocyte reservoir in diving-related interventions. J Appl Physiol 92(5):2071–2079PubMedCrossRef
Fagoni N, Sivieri A, Antonutto G, Moia C, Taboni A, Bringard A, Ferretti G (2015) Cardiovascular responses to dry resting apnoeas in elite divers while breathing pure oxygen. Respir Physiol Neurobiol 219:1–8PubMedCrossRef
Ferretti G (2001) Extreme human breath-hold diving. J Appl Physiol 84(4):254–271
Ferretti G, Costa M, Ferrigno M, Grassi B, Marconi C, Lundgren CE, Cerretelli P (1991) Alveolar gas composition and exchange during deep breath-hold diving and dry breath holds in elite divers. J Appl Physiol 70(4):794–802PubMedCrossRef
Ferretti G, Costa M, Moroni R, Ranieri P, Butti F, Sponsiello N (2012) Lung volumes of extreme breath-hold divers. Sport Sci Health 7:55–59CrossRef
Findley LJ, Ries AL, Tisi GM, Wagner PD (1983) Hypoxemia during apnea in normal subjects: mechanisms and impact of lung volume. J Appl Physiol Respir Environ Exerc Physiol 55(6):1777–1783PubMed
Flume PA, Eldridge FL, Edwards LJ, Mattison LE (1996) Relief of the “air hunger” of breathholding. A role for pulmonary stretch receptors. Respir Physiol 103:221–232PubMedCrossRef
Foster GE, Sheel AW (2005) The human diving response, its function, and its control. Scand J Med Sci Sports 15(1):3–12PubMedCrossRef
Freire RC, Nardi AE (2012) Panic disorder and the respiratory system: clinical subtype and challenge tests. Braz J Psychiatry 34(1):32–34CrossRef
Guyenet PG, Abbott SB, Stornetta RL (2013) The respiratory chemoreception conundrum: light at the end of the tunnel? Brain Res 20(1511):126–137CrossRef
Heath JR, Irwin CJ (1968) An increase in breath-hold time appearing after breath-holding. Respir Physiol 4:73–77PubMedCrossRef
Hoiland RL, Ainslie PN, Bain AR, MacLeod DB, Stembridge M, Drvis I, Madden D, Barak O, MacLeod DM, Dujic Z (2017) β1-Blockade increases maximal apnea duration in elite breath-hold divers. J Appl Physiol 122(4):899–906PubMedCrossRef
Hudson AL, Raux M, Similowski T, Niérat M (2018) The relationship between respiratory-related premotor potentials and small perturbations in ventilation. Front Physiol 9:621PubMedPubMedCentralCrossRef
Inoue H, Yamauchi K, Kobayashi H, Shikanai T, Nakamura Y, Satoh J, Kohno N, Mishima M, Sasaki H, Hildebrandt J (2009) A new breath-holding test may noninvasively reveal early lung abnormalities caused by smoking and/or obesity. Chest 136(2):545–553PubMedCrossRef
Kleinfeld D, Deschênes M, Wang F, Moore JD (2014) More than a rhythm of life: breathing as a binder of orofacial sensation. Nat Neurosci 17(5):647–651PubMedPubMedCentralCrossRef
Klimesch W (2009) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29(2–3):169–195
Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263–297PubMedCrossRef
Lemaître F, Polin D, Joulia F, Boutry A, Le Pessot D, Chollet D, Tourny-Chollet C (2007) Physiological responses to repeated apneas in underwater hockey players and controls. Undersea Hyperb Med 34(6):407–414PubMed
Lemaître F, Clua E, Andréani B, Castres I, Chollet D (2010) Ventilatory function in breath-hold divers: effect of glossopharyngeal insufflation. Eur J Appl Physiol 108(4):741–747PubMedCrossRef
Lin YC, Lally DA, Moore TO, Hong SK (1974) Physiological and conventional breath-hold breaking points. J Appl Physiol 37(3):291–296PubMedCrossRef
Lindholm P, Lundgren CE (2009) The physiology and pathophysiology of human breath-hold diving. J Appl Physiol 106(1):284–292PubMedCrossRef
Lindholm P, Nyrén S (2005) Studies on inspiratory and expiratory glossopharyngeal breathing in breath-hold divers employing magnetic resonance imaging and spirometry. Eur J Appl Physiol 94(5–6):646–651PubMedCrossRef
Loring SH, O’Donnell CR, Butler JP, Lindholm P, Jacobson F, Ferrigno M (2007) Transpulmonary pressures and lung mechanics with glossopharyngeal insufflation and exsufflation beyond normal lung volumes in competitive breath-hold divers. J Appl Physiol 102(3):841–846PubMedCrossRef
Ma X, Yue ZQ, Gong ZQ, Zhang H, Duan NY, Shi YT, Wei GX, Li YF (2017) The effect of diaphragmatic breathing on attention, negative affect and stress in healthy adults. Front Psychol 8:874PubMedPubMedCentralCrossRef
Macefield G, Gandevia SC (1991) The cortical drive to human respiratory muscles in the awake state assessed by premotor cerebral potentials. J Physiol 439:545–558PubMedPubMedCentralCrossRef
Malathi A, Damodaran A (1999) Stress due to exams in medical students—role of yoga. Indian J Physiol Pharmacol 43(2):218–224PubMed
Marek W, Muckenhoff K, Prabhakar NR (2008) Significance of pulmonary vagal afferents for respiratory muscle activity in the cat. J Physiol Pharmacol 6:407
Martelli D, Stanić D, Dutschmann M (2013) The emerging role of the parabrachial complex in the generation of wakefulness drive and its implication for respiratory control. Respir Physiol Neurobiol 188(3):318–323PubMedCrossRef
Martin C, Ravel N (2014) Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks? Front Behav Neurosci 23(8):218
Menicucci D, Artoni F, Bedini R, Pingitore A, Passera M, Landi A, L’Abbate A, Sebastiani L, Gemignani A (2014) Brain responses to emotional stimuli during breath holding and hypoxia: an approach based on the independent component analysis. Brain Topogr 27(6):771–785PubMedCrossRef
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202PubMedCrossRef
Moral Y, Robertson NJ, Goni-de-Cerio F, Alonso-Alconada D (2019) Neonatal hypoxia-ischemia: cellular and molecular brain damage and therapeutic modulation of neurogenesis. Rev Neurol 68(1):23–36PubMed
Nannini LJ, Zaietta GA, Guerrera AJ, Varela JA, Fernández OM, Flores DM (2007) Breath-holding test in subjects with near-fatal asthma. A new index for dyspnea perception. Respir Med 101(2):246–253PubMedCrossRef
Napadow V, Dhond R, Conti G, Makris N, Bronw EN, Barbieri R (2008) Brain correlates of autonomic modulation: combining heart rate variability with FMRI. Neuroimage 42(1):169–177PubMedCrossRef
Netz Y, Lidor R (2017) Mood alterations in mindful versus aerobic exercise modes. J Psychol 137(5):405–419CrossRef
Nishino T (2009) Pathophysiology of dyspnea evaluated by breath-holding test: studies of furosemide treatment. Respir Physiol Neurobiol 167(1):20–25PubMedCrossRef
Nishino T, Sugimori K, Ishikawa T (1996) Changes in the period of no respiratory sensation and total breath-holding time in successive breath-holding trials. Clin Sci 91(6):755–761CrossRef
Palada I, Bakovic D, Valic Z, Obad A, Ivancev V, Eterovic D, Shoemaker JK, Dujic Z (2008) Restoration of hemodynamics in apnea struggle phase in association with involuntary breathing movements. Respir Physiol Neurobiol 161(2):174–181PubMedCrossRef
Papadelis C, Kourtidou-Papadeli C, Bamidis PD, Maglaveras N, Pappas K (2017) The effect of hypobaric hypoxia on multichannel EEG signal complexity. Clin Neurophysiol 18(1):31–52CrossRef
Patrician A, Gasho C, Spajić B, Caldwell HG, Baković-Kramaric D, Barak O, Drviš I, Dujić Ž, Ainslie PN (2021) Breath-hold diving beyond 100 meters-cardiopulmonary responses in world-champion divers. J Appl Physiol 130(5):1345–1350PubMedCrossRef
Perciavalle V, Blandini M, Fecarotta P, Buscemi A, Di Corrado D, Bertolo L, Fichera F, Coco M (2017) The role of deep breathing on stress. Neurol Sci 38(3):451–458PubMedCrossRef
Perini R, Tironi A, Gheza A, Butti F, Moia C, Ferretti G (2008) Heart rate and blood pressure time courses during prolonged dry apnoea in breath-hold divers. Eur J Appl Physiol 104(1):1–7PubMedCrossRef
Perini R, Gheza A, Moia C, Sponsiello N, Ferretti G (2010) Cardiovascular time courses during prolonged immersed static apnoea. Eur J Appl Physiol 110(2):277–283PubMedCrossRef
Priovoulos N, Poser BA, Ivanov D, Verhey FRJ, Jacobs HIL (2019) In vivo imaging of the nucleus of the solitary tract with Magnetization Transfer at 7 Tesla. Neuroimage 1(201):116071CrossRef
Rahn H, Bahnson HT, Muxworthy JF, Hagen JM (1953) Adaptation to high altitude: changes in breath-holding time. J Appl Physiol 6(3):154–157PubMedCrossRef
Rassovsky Y, Abrams K, Kushner MG (2006) Suffocation and respiratory responses to carbon dioxide and breath holding challenges in individuals with panic disorder. J Psychosom Res 60(3):291–298PubMedCrossRef
Ratmanova P, Semenyuk R, Popov D, Kuznetsov S, Zelenkova I, Napalkov D, Vinogradova O (2016) Prolonged dry apnoea: effects on brain activity and physiological functions in breath-hold divers and non-divers. Eur J Appl Physiol 116(7):1367–1377PubMedCrossRef
Ridderinkhof KR, Van Den Wildenberg WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56(2):29–40CrossRef
Romano TG, Correia MD, Mendes PV, Zampieri FG, Maciel AT, Park M (2016) Metabolic acid-base adaptation triggered by acute persistent hypercapnia in mechanically ventilated patients with acute respiratory distress syndrome. Rev Bras Ter Intensiva 28(1):19–26PubMedPubMedCentralCrossRef
Schagatay E, Andersson J (1998) Diving response and apneic time in humans. Undersea Hyperb Med 25(1):13–19PubMed
Schagatay E, Van Kampen M, Andersson J (1999) Effects of repeated apneas on apneic time and diving response in non-divers. Undersea Hyperb Med 26:143–149PubMed
Schagatay E, Van Kampen M, Emanuelsson S, Holm B (2000) Effects of physical and apnea training on apneic time and the diving response in humans. Eur J Appl Physiol 82(3):161–169PubMedCrossRef
Schagatay E, Andersson JP, Hallén M, Pålsson B (2001) Selected contribution: role of spleen emptying in prolonging apneas in humans. J Appl Physiol 90(4):1623–1629PubMedCrossRef
Schipke JD, Kelm M, Siegmund K, Muth T, Sievers B, Steiner S (2015) “Lung packing” in breath hold-diving: an impressive case of pulmo-cardiac interaction. Respir Med Case Rep 16(16):120–121PubMedPubMedCentral
Sinha M, Sinha R, Ghate J, Sarnik G (2020) Impact of altered breathing patterns on interaction of EEG and heart rate variability. Ann Neurosci 27(2):67–77PubMedPubMedCentralCrossRef
Sivieri A, Fagoni N, Bringard A, Capogrosso M, Perini R, Ferretti G (2015) A beat-by-beat analysis of cardiovascular responses to dry resting and exercise apnoeas in elite divers. Eur J Appl Physiol 115(1):119–128PubMedCrossRef
Steinberg F, Pixa NH, Doppelmayr M (2017) Electroencephalographic alpha activity modulations induced by breath-holding in apnea divers and non-divers. Physiol Behav 179(1):2–26
Sterba JA, Lundgren CE (1988) Breath-hold duration in man and the diving response induced by face immersion. Undersea Biomed Res 15(5):361–375PubMed
Taboni A, Vinetti G, Bruseghini P, Camelio S, D’Elia M, Moia C, Ferretti G, Fagoni N (2018) Cardiovascular responses to dry apnoeas at exercise in air and in pure oxygen. Respir Physiol Neurobiol 255:17–21PubMedCrossRef
Taboni A, Fagoni N, Fontolliet T, Grasso GS, Moia C, Vinetti G, Ferretti G (2020) Breath holding as an example of extreme hypoventilation: experimental testing of a new model describing alveolar gas pathways. Exp Physiol 105(12):2216–2225PubMedCrossRef
Thayer JF, Lane RD (2009) Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 33(2):81–88PubMedCrossRef
Thornton JM, Guz A, Murphy K, Griffith AR, Pedersen DL, Kardos A, Leff A, Adams L, Casadei B, Paterson DJ (2001) Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans. J Physiol 533(Pt 3):823–836PubMedPubMedCentralCrossRef
Tort ABL, Brankack J, Draguhn A (2018) Respiration-entrained brain rhythms are global but often overlooked. Trends Neurosci 41(4):186–197PubMedCrossRef
Tremoureux L, Raux M, Ranohavimparany A, Morélot-Panzini C, Pouget P, Similowski T (2014) Electroencephalographic evidence for a respiratory-related cortical activity specific of the preparation of prephonatory breaths. Respir Physiol Neurobiol 1(204):64–70CrossRef
Viecili RB, Sanches PR, Silva DR, Silva DP, Muller AF, Barreto SS (2011) Bronchodilator effect on maximal breath-hold time in patients with obstructive lung disease. J Bras Pneumol 37(6):745–751PubMedCrossRef
Viecili RB, Silva DR, Sanches PRS, Müller AF, Silva DP, Barreto SSM (2012) Real-time measurement of maximal voluntary breath-holding time in patients with obstructive ventilatory defects and normal controls. J Pulmon Resp Med 2:5CrossRef
Walterspacher S, Scholz T, Tetzlaff K, Sorichter S (2011) Breath-hold diving: respiratory function on the longer term. Med Sci Sports Exerc 43(7):1214–1219PubMedCrossRef
Whitelaw WA, McBride B, Ford GT (1987) Effect of lung volume on breath holding. J Appl Physiol 62(5):1962–1969PubMedCrossRef
Zelano C, Jiang H, Zhou G, Arora N, Schuele S, Rosenow J, Gottfried JA (2016) Nasal respiration entrains human limbic oscillations and modulates cognitive function. J Neurosci 36(49):12448–12467PubMedPubMedCentralCrossRef
Zoccal DB, Furuya WI, Bassi M, Colombari DS, Colombari E (2014) The nucleus of the solitary tract and the coordination of respiratory and sympathetic activities. Front Physiol 25(5):238
Metadata
Title
Breath-holding as model for the evaluation of EEG signal during respiratory distress
Authors
Lucas de Jesus Alves Ribeiro
Victor Hugo do Vale Bastos
Marcelo Coertjens
Publication date
17-12-2023
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 3/2024
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-023-05379-x

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