Skip to main content
Top
Published in: Sleep and Breathing 2/2022

07-07-2021 | Sleep Apnea | Sleep Breathing Physiology and Disorders • Original Article

Interactions of central and autonomic nervous systems in patients with sleep apnea–hypopnea syndrome during sleep

Authors: Tingting Wang, Juan Yang, Yingjie Song, Feng Pang, Xinwen Guo, Yuxi Luo

Published in: Sleep and Breathing | Issue 2/2022

Login to get access

Abstract

Purpose

Sleep apnea–hypopnea syndrome (SAHS) is an independent risk factor for various cardiovascular and cerebrovascular diseases, but the underlying relationship of its physiological subsystems remains unclear. Thus, we aimed to investigate the effect of SAHS on central and autonomic nervous system (CNS-ANS) interactions during sleep.

Methods

Thirty-five patients with SAHS and 19 healthy age-matched controls underwent overnight polysomnography. The absolute spectral powers of five frequency bands from six EEG channels and ECG morphological features (HR, PR interval, QT interval) were calculated. Multivariable transfer entropy was applied to analyze the differences of the CNS-ANS network interactions between patients with SAHS of different severities and healthy controls during deep, light, and rapid eye movement sleep.

Results

The CNS-ANS network interacted bidirectionally in all researched groups, with the cardiac information modulating the brain activity. The information strength from QT to most EEG components and PR to some EEG components was significantly affected by SAHS severity during light sleep, which indicates the coupling features of QT-brain nodes are important indicators. The driver effects from the β-band significantly increased in patients with SAHS.

Conclusions

Respiratory events may be the main reason for the CNS-ANS interaction changes in SAHS. These findings help explain the physiological regulation process of SAHS and provide valuable information for analysis of the development of SAHS-related cardiovascular and chronic diseases.
Appendix
Available only for authorised users
Glossary
RR
the interval between two adjacent R peaks;
PR
the interval from the start of the P-wave to the start of the QRS complex;
QT
the interval from the start of the QRS complex to the end of the T-wave.
Literature
2.
go back to reference Benjafield AV, Ayas NT, Eastwood PR, Heinzer R, Ip MSM, Morrell MJ et al (2019) Estimation of the global prevalence and burden of obstructive sleep apnoea: a literature-based analysis. Lancet Respir Med 7(8):687–698PubMedPubMedCentralCrossRef Benjafield AV, Ayas NT, Eastwood PR, Heinzer R, Ip MSM, Morrell MJ et al (2019) Estimation of the global prevalence and burden of obstructive sleep apnoea: a literature-based analysis. Lancet Respir Med 7(8):687–698PubMedPubMedCentralCrossRef
3.
go back to reference Ott SR, Korostovtseva L, Schmidt M, Horvath T, Brill AK, Bassetti CL (2017) Sleep-disordered breathing: clinical features, pathophysiology and diagnosis. Swiss Med Wkly 147:w14436PubMed Ott SR, Korostovtseva L, Schmidt M, Horvath T, Brill AK, Bassetti CL (2017) Sleep-disordered breathing: clinical features, pathophysiology and diagnosis. Swiss Med Wkly 147:w14436PubMed
4.
go back to reference Sarkar P, Mukherjee S, Chai-Coetzer CL, McEvoy RD (2018) The epidemiology of obstructive sleep apnoea and cardiovascular disease. J Thorac Dis 10(Suppl 34):S4189–S4200PubMedPubMedCentralCrossRef Sarkar P, Mukherjee S, Chai-Coetzer CL, McEvoy RD (2018) The epidemiology of obstructive sleep apnoea and cardiovascular disease. J Thorac Dis 10(Suppl 34):S4189–S4200PubMedPubMedCentralCrossRef
6.
go back to reference Di Fusco SA, Pignalberi C, Santini L, Colivicchi F, Santini M (2020) Arrhythmias and sleep apnea: physiopathologic link and clinical implications. J Interv Card Electrophysiol 57(3):387–397PubMedCrossRef Di Fusco SA, Pignalberi C, Santini L, Colivicchi F, Santini M (2020) Arrhythmias and sleep apnea: physiopathologic link and clinical implications. J Interv Card Electrophysiol 57(3):387–397PubMedCrossRef
7.
go back to reference Hla KM, Young T, Hagen EW, Stein JH, Finn LA, Nieto FJ et al (2015) Coronary heart disease incidence in sleep disordered breathing: the Wisconsin Sleep Cohort Study. Sleep 38(5):677–684PubMedPubMedCentralCrossRef Hla KM, Young T, Hagen EW, Stein JH, Finn LA, Nieto FJ et al (2015) Coronary heart disease incidence in sleep disordered breathing: the Wisconsin Sleep Cohort Study. Sleep 38(5):677–684PubMedPubMedCentralCrossRef
8.
go back to reference Parati G, Lombardi C, Castagna F, Mattaliano P, Filardi PP, Agostoni P et al (2016) Heart failure and sleep disorders. Nat Rev Cardiol 13(7):389–403PubMedCrossRef Parati G, Lombardi C, Castagna F, Mattaliano P, Filardi PP, Agostoni P et al (2016) Heart failure and sleep disorders. Nat Rev Cardiol 13(7):389–403PubMedCrossRef
10.
go back to reference Redline S, Kirchner L, Quan SF, Gottlieb DJ, Kapur V, Newman A (2004) The effects of age, sex, ethnicity, and sleep-disordered breathing on sleep architecture. Arch Intern Med 164(4):406–418PubMedCrossRef Redline S, Kirchner L, Quan SF, Gottlieb DJ, Kapur V, Newman A (2004) The effects of age, sex, ethnicity, and sleep-disordered breathing on sleep architecture. Arch Intern Med 164(4):406–418PubMedCrossRef
11.
go back to reference Zeng L, Liang J, Liao Y, Zhou G, Zhang X, Luo Y (2019) Variation of electrocardiogram features across sleep stages in healthy controls and in patients with sleep apnea hypopnea syndrome. Int Heart J 60(1):121–128PubMedCrossRef Zeng L, Liang J, Liao Y, Zhou G, Zhang X, Luo Y (2019) Variation of electrocardiogram features across sleep stages in healthy controls and in patients with sleep apnea hypopnea syndrome. Int Heart J 60(1):121–128PubMedCrossRef
12.
go back to reference Liang J, Zhang X, He X, Ling L, Zeng C, Luo Y (2018) The independent and combined effects of respiratory events and cortical arousals on the autonomic nervous system across sleep stages. Sleep Breath 22(4):1161–1168PubMedCrossRef Liang J, Zhang X, He X, Ling L, Zeng C, Luo Y (2018) The independent and combined effects of respiratory events and cortical arousals on the autonomic nervous system across sleep stages. Sleep Breath 22(4):1161–1168PubMedCrossRef
13.
go back to reference Liang J, Zhang X, Luo Y, Wang T, Sun L, Huang S (2018) The impact of respiratory events on the autonomic nervous system during sleep. Int Heart J 59(2):378–386PubMedCrossRef Liang J, Zhang X, Luo Y, Wang T, Sun L, Huang S (2018) The impact of respiratory events on the autonomic nervous system during sleep. Int Heart J 59(2):378–386PubMedCrossRef
14.
go back to reference Zambotti MD, Trinder J, Silvani A, Colrain IM, Baker FC (2018) Dynamic coupling between the central and autonomic nervous systems during sleep: a review. Neurosci Biobehav Rev 90:84–103PubMedPubMedCentralCrossRef Zambotti MD, Trinder J, Silvani A, Colrain IM, Baker FC (2018) Dynamic coupling between the central and autonomic nervous systems during sleep: a review. Neurosci Biobehav Rev 90:84–103PubMedPubMedCentralCrossRef
15.
go back to reference Silvani A, Calandra-Buonaura G, Dampney RA, Cortelli P (2016) Brain-heart interactions: physiology and clinical implications. Philos Trans A Math Phys Eng Sci 374(2067) Silvani A, Calandra-Buonaura G, Dampney RA, Cortelli P (2016) Brain-heart interactions: physiology and clinical implications. Philos Trans A Math Phys Eng Sci 374(2067)
16.
go back to reference Jurysta F, Lanquart JP, van de Borne P, Migeotte PF (2006) The link between cardiac autonomic activity and sleep delta power is altered in men with sleep apnea-hypopnea syndrome. Am J Physiol-Reg I 291(4):R1165–R1171 Jurysta F, Lanquart JP, van de Borne P, Migeotte PF (2006) The link between cardiac autonomic activity and sleep delta power is altered in men with sleep apnea-hypopnea syndrome. Am J Physiol-Reg I 291(4):R1165–R1171
17.
go back to reference Rothenberger SD, Krafty RT, Taylor BJ, Cribbet MR, Thayer JF, Buysse DJ et al (2015) Time-varying correlations between delta EEG power and heart rate variability in midlife women: the SWAN Sleep Study. Psychophysiology 52(4):572–584PubMedCrossRef Rothenberger SD, Krafty RT, Taylor BJ, Cribbet MR, Thayer JF, Buysse DJ et al (2015) Time-varying correlations between delta EEG power and heart rate variability in midlife women: the SWAN Sleep Study. Psychophysiology 52(4):572–584PubMedCrossRef
18.
go back to reference Orjuela-Canon AD, Cerquera A, Freund JA, Julia-Serda G, Ravelo-Garcia AG (2020) Sleep apnea: tracking effects of a first session of CPAP therapy by means of Granger causality. Comput Methods Programs Biomed 187:105235PubMedCrossRef Orjuela-Canon AD, Cerquera A, Freund JA, Julia-Serda G, Ravelo-Garcia AG (2020) Sleep apnea: tracking effects of a first session of CPAP therapy by means of Granger causality. Comput Methods Programs Biomed 187:105235PubMedCrossRef
19.
go back to reference Knyazev GG (2012) EEG delta oscillations as a correlate of basic homeostatic and motivational processes. Neurosci Biobehav Rev 36(1):677–695PubMedCrossRef Knyazev GG (2012) EEG delta oscillations as a correlate of basic homeostatic and motivational processes. Neurosci Biobehav Rev 36(1):677–695PubMedCrossRef
20.
21.
go back to reference Yang J, Pan Y, Wang T, Zhang X, Wen J, Luo Y (2020) Sleep-dependent directional interactions of the central nervous system-cardiorespiratory network. IEEE Trans Biomed Eng 68(2):639–649CrossRef Yang J, Pan Y, Wang T, Zhang X, Wen J, Luo Y (2020) Sleep-dependent directional interactions of the central nervous system-cardiorespiratory network. IEEE Trans Biomed Eng 68(2):639–649CrossRef
22.
go back to reference Perlis ML, Smith MT, Andrews PJ, Orff H, Giles DE (2001) Beta/gamma EEG activity in patients with primary and secondary insomnia and good sleeper controls. Sleep 24(1):110–117PubMedCrossRef Perlis ML, Smith MT, Andrews PJ, Orff H, Giles DE (2001) Beta/gamma EEG activity in patients with primary and secondary insomnia and good sleeper controls. Sleep 24(1):110–117PubMedCrossRef
23.
go back to reference Knyazev GG (2007) Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci Biobehav Rev 31(3):377–395PubMedCrossRef Knyazev GG (2007) Motivation, emotion, and their inhibitory control mirrored in brain oscillations. Neurosci Biobehav Rev 31(3):377–395PubMedCrossRef
24.
go back to reference Jurysta F, van de Borne P, Migeotte PF, Dumont M, Lanquart JP, Degaute JP et al (2003) A study of the dynamic interactions between sleep EEG and heart rate variability in healthy young men. Clin Neurophysiol 114(11):2146–2155PubMedCrossRef Jurysta F, van de Borne P, Migeotte PF, Dumont M, Lanquart JP, Degaute JP et al (2003) A study of the dynamic interactions between sleep EEG and heart rate variability in healthy young men. Clin Neurophysiol 114(11):2146–2155PubMedCrossRef
26.
go back to reference Vicente R, Wibral M, Lindner M, Pipa G (2011) Transfer entropy-a model-free measure of effective connectivity for the neurosciences. J Comput Neurosci 30(1):45–67PubMedCrossRef Vicente R, Wibral M, Lindner M, Pipa G (2011) Transfer entropy-a model-free measure of effective connectivity for the neurosciences. J Comput Neurosci 30(1):45–67PubMedCrossRef
27.
go back to reference Schulz S, Haueisen J, Bär KJ, Voss A (2019) Altered causal coupling pathways within the central-autonomic-network in patients suffering from schizophrenia. Entropy 21(8):733PubMedCentralCrossRef Schulz S, Haueisen J, Bär KJ, Voss A (2019) Altered causal coupling pathways within the central-autonomic-network in patients suffering from schizophrenia. Entropy 21(8):733PubMedCentralCrossRef
28.
go back to reference Montalto A, Faes L, Marinazzo D (2014) MuTE: a MATLAB toolbox to compare established and novel estimators of the multivariate transfer entropy. PLoS One 9(10):e109462PubMedPubMedCentralCrossRef Montalto A, Faes L, Marinazzo D (2014) MuTE: a MATLAB toolbox to compare established and novel estimators of the multivariate transfer entropy. PLoS One 9(10):e109462PubMedPubMedCentralCrossRef
29.
go back to reference Fink AM, Bronas UG, Calik MW (2018) Autonomic regulation during sleep and wakefulness: a review with implications for defining the pathophysiology of neurological disorders. Clin Auton Res 28(6):509–518PubMedPubMedCentralCrossRef Fink AM, Bronas UG, Calik MW (2018) Autonomic regulation during sleep and wakefulness: a review with implications for defining the pathophysiology of neurological disorders. Clin Auton Res 28(6):509–518PubMedPubMedCentralCrossRef
30.
go back to reference Abdullah H, Maddage N, Cosic I, Cvetkovic D (2010) Brain and heart interaction during sleep in the healthy and sleep apnoea. Paper presented at the 2010 IEEE EMBS Conference on Biomedical Engineering and Sciences (IECBES 2010), Kuala Lumpur, Malaysia, 30 Nov-2 Dec Abdullah H, Maddage N, Cosic I, Cvetkovic D (2010) Brain and heart interaction during sleep in the healthy and sleep apnoea. Paper presented at the 2010 IEEE EMBS Conference on Biomedical Engineering and Sciences (IECBES 2010), Kuala Lumpur, Malaysia, 30 Nov-2 Dec
31.
go back to reference Khandoker AH, Karmakar CK, Palaniswami M (2008) Analysis of coherence between sleep EEG and ECG signals during and after obstructive sleep apnea events. Paper presented at the 30th Annual International Conference of the IEEE-Engineering-in-Medicine-and-Biology-Society, Vancouver, Canada, 20–24 Aug Khandoker AH, Karmakar CK, Palaniswami M (2008) Analysis of coherence between sleep EEG and ECG signals during and after obstructive sleep apnea events. Paper presented at the 30th Annual International Conference of the IEEE-Engineering-in-Medicine-and-Biology-Society, Vancouver, Canada, 20–24 Aug
32.
go back to reference Long X, Arends JB, Aarts RM, Haakma R, Fonseca P, Rolink J (2015) Time delay between cardiac and brain activity during sleep transitions. Appl Phys Lett 106(14):4CrossRef Long X, Arends JB, Aarts RM, Haakma R, Fonseca P, Rolink J (2015) Time delay between cardiac and brain activity during sleep transitions. Appl Phys Lett 106(14):4CrossRef
33.
go back to reference Yan J, Zhang X, Yen C-W, Sun L, Yu E, Luo Y (2016) Role of electroencephalogram and oxygen saturation in the induction mechanism of arousal for obstructive sleep apnea-hypopnea syndrome patients. Biol Rhythm Res 47(4):483–495CrossRef Yan J, Zhang X, Yen C-W, Sun L, Yu E, Luo Y (2016) Role of electroencephalogram and oxygen saturation in the induction mechanism of arousal for obstructive sleep apnea-hypopnea syndrome patients. Biol Rhythm Res 47(4):483–495CrossRef
34.
go back to reference Zhou G, Pan Y, Liao Y, Liang J, Zhang X, Luo Y (2020) Short-term impact of sleep apnea/hypopnea on the interaction between various cortical areas. Clin EEG Neurosci 52(4):296–306PubMedCrossRef Zhou G, Pan Y, Liao Y, Liang J, Zhang X, Luo Y (2020) Short-term impact of sleep apnea/hypopnea on the interaction between various cortical areas. Clin EEG Neurosci 52(4):296–306PubMedCrossRef
35.
go back to reference Huang S, Wang T, Zhang X, Yen CW, Liang J, Zeng L et al (2018) The correlations between electroencephalogram frequency components and restoration of stable breathing from respiratory events in sleep apnea hypopnea syndrome. Respir Physiol Neurobiol 258:91–97PubMedCrossRef Huang S, Wang T, Zhang X, Yen CW, Liang J, Zeng L et al (2018) The correlations between electroencephalogram frequency components and restoration of stable breathing from respiratory events in sleep apnea hypopnea syndrome. Respir Physiol Neurobiol 258:91–97PubMedCrossRef
36.
go back to reference Gami AS, Olson EJ, Shen WK, Wright RS, Ballman KV, Hodge DO et al (2013) Obstructive sleep apnea and the risk of sudden cardiac death: a longitudinal study of 10,701 adults. J Am Coll Cardiol 62(7):610–616PubMedCrossRef Gami AS, Olson EJ, Shen WK, Wright RS, Ballman KV, Hodge DO et al (2013) Obstructive sleep apnea and the risk of sudden cardiac death: a longitudinal study of 10,701 adults. J Am Coll Cardiol 62(7):610–616PubMedCrossRef
37.
go back to reference Seyerle AA, Lin HJ, Gogarten SM, Stilp A, Giraldez RM, Soliman E et al (2018) Genome-wide association study of PR interval in Hispanics/Latinos identifies novel locus at ID2. Heart 104(11):904–911PubMedCrossRef Seyerle AA, Lin HJ, Gogarten SM, Stilp A, Giraldez RM, Soliman E et al (2018) Genome-wide association study of PR interval in Hispanics/Latinos identifies novel locus at ID2. Heart 104(11):904–911PubMedCrossRef
38.
go back to reference Neyroud N, Maison-Blanche P, Denjoy I, Chevret S, Donger C, Dausse E et al (1998) Diagnostic performance of QT interval variables form 24-h electrocardiography in the long QT syndrome. Eur Heart J 19(1):158–165PubMedCrossRef Neyroud N, Maison-Blanche P, Denjoy I, Chevret S, Donger C, Dausse E et al (1998) Diagnostic performance of QT interval variables form 24-h electrocardiography in the long QT syndrome. Eur Heart J 19(1):158–165PubMedCrossRef
39.
go back to reference Browne KF, Prystowsky E, Heger JJ, Chilson DA, Zipes DP (1983) Prolongation of the Q-T interval in man during sleep. AM J Cardiol 52(1):55–59PubMedCrossRef Browne KF, Prystowsky E, Heger JJ, Chilson DA, Zipes DP (1983) Prolongation of the Q-T interval in man during sleep. AM J Cardiol 52(1):55–59PubMedCrossRef
40.
go back to reference Roche F, Gaspoz JM, Court-Fortune I, Costes F, Geyssant A, Duverney D et al (2003) Alteration of QT rate dependence reflects cardiac autonomic imbalance in patients with obstructive sleep apnea syndrome. Pace-Pacing Clin Electrophysiol 26(7):1446–1453PubMedCrossRef Roche F, Gaspoz JM, Court-Fortune I, Costes F, Geyssant A, Duverney D et al (2003) Alteration of QT rate dependence reflects cardiac autonomic imbalance in patients with obstructive sleep apnea syndrome. Pace-Pacing Clin Electrophysiol 26(7):1446–1453PubMedCrossRef
41.
go back to reference Gillis AM, Stoohs R, Guilleminault C (1991) Changes in the QT interval during obstructive sleep apnea. Sleep 14(4):346–350PubMedCrossRef Gillis AM, Stoohs R, Guilleminault C (1991) Changes in the QT interval during obstructive sleep apnea. Sleep 14(4):346–350PubMedCrossRef
42.
go back to reference Poliakova N, Despres JP, Bergeron J, Almeras N, Tremblay A, Poirier P (2012) Influence of obesity indices, metabolic parameters and age on cardiac autonomic function in abdominally obese men. Metabolism 61(9):1270–1279PubMedCrossRef Poliakova N, Despres JP, Bergeron J, Almeras N, Tremblay A, Poirier P (2012) Influence of obesity indices, metabolic parameters and age on cardiac autonomic function in abdominally obese men. Metabolism 61(9):1270–1279PubMedCrossRef
Metadata
Title
Interactions of central and autonomic nervous systems in patients with sleep apnea–hypopnea syndrome during sleep
Authors
Tingting Wang
Juan Yang
Yingjie Song
Feng Pang
Xinwen Guo
Yuxi Luo
Publication date
07-07-2021
Publisher
Springer International Publishing
Published in
Sleep and Breathing / Issue 2/2022
Print ISSN: 1520-9512
Electronic ISSN: 1522-1709
DOI
https://doi.org/10.1007/s11325-021-02429-6

Other articles of this Issue 2/2022

Sleep and Breathing 2/2022 Go to the issue

Sleep Breathing Physiology and Disorders • Original Article

Upper airway collapse characteristics in adult patients with OSA and previous tonsillectomy