Investigation of Heartbeat Evoked Potential (HEP) Response During Different Stages of Sleep in Sleep Disorders
Abstract
Purpose: Interoceptions are a combination of sensation, integration, and interpretation of internal bodily signals. Interoceptions are bidirectionally related to the human being mental and physiological health, and well-being. Sleep and different interoceptive modalities are proven to share common relations.
Heartbeat Evoked Potential (HEP) is known as a robust readout to interoceptive processes. In this study, we focused on the relation between HEP modulations and sleep-related disorders.
Materials and Methods: We investigated four different sleep-related disorders, including insomnia, rapid eye movement behavior disorder, periodic limb movements and nocturnal frontal lobe epilepsy, and provided HEP signals of multiple Electroencephalogram (EEG) channels over the right hemisphere to compare these disorders with the control group. Here, we investigated and compared the results of 35 subjects, including seven subjects for the control group and seven subjects for each of above-mentioned sleep disorders.
Results: By comparing HEP responses of the control group with sleep-related patients’ groups, statistically significant HEP differences were detected over right hemisphere EEG channels, including FP2, F4, C4, P4, and O2 channels. These significant differences were also observed over the grand average HEP amplitude activity of channels over the right hemisphere in the sleep-related disorders as well.
Conclusion: Our results between the control group and groups of patients suffering from sleep-related disorders demonstrated that during different stages of sleep, HEPs show significant differences over multiple right hemisphere EEG channels. Interestingly, by comparing different sleep disorders with each other, we observed that each of these HEP differences’ patterns over specific channels and during certain sleep stages bear considerable resemblances to each other.
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30- G Dirlich, L Vogl, M Plaschke, and F Strian, "Cardiac field effects on the EEG." Electroencephalography and clinical neurophysiology, Vol. 102 (No. 4), pp. 307-15, (1997).
31- Olga Pollatos, Wladimir Kirsch, and Rainer Schandry, "On the relationship between interoceptive awareness, emotional experience, and brain processes." Cognitive brain research, Vol. 25 (No. 3), pp. 948-62, (2005).
32- Eric Maris and Robert Oostenveld, "Nonparametric statistical testing of EEG-and MEG-data." Journal of neuroscience methods, Vol. 164 (No. 1), pp. 177-90, (2007).
33- Hugo D Critchley, Stefan Wiens, Pia Rotshtein, Arne Öhman, and Raymond J Dolan, "Neural systems supporting interoceptive awareness." Nature neuroscience, Vol. 7 (No. 2), pp. 189-95, (2004).
34- Ralph Adolphs, Hanna Damasio, Daniel Tranel, Greg Cooper, and Antonio R Damasio, "A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping." Journal of neuroscience, Vol. 20 (No. 7), pp. 2683-90, (2000).
35- Yishul Wei et al., "I keep a close watch on this heart of mine: increased interoception in insomnia." Sleep, Vol. 39 (No. 12), pp. 2113-24, (2016).
36- Ronald C Hamdy et al., "Insomnia and mild cognitive impairment." Gerontology and Geriatric Medicine, Vol. 4p. 2333721418778421, (2018).
37- Angela Zhang, Lei Xing, James Zou, and Joseph C Wu, "Shifting machine learning for healthcare from development to deployment and from models to data." Nature Biomedical Engineering, pp. 1-16, (2022).
2- Sahib S Khalsa et al., "Interoception and mental health: a roadmap." Biological psychiatry: cognitive neuroscience and neuroimaging, Vol. 3 (No. 6), pp. 501-13, (2018).
3- Yishul Wei and Eus JW Van Someren, "Interoception relates to sleep and sleep disorders." Current Opinion in Behavioral Sciences, Vol. 33pp. 1-7, (2020).
4- John H Peever and Barry J Sessle, "Sensory and motor processing during sleep and wakefulness." in Principles and practice of sleep medicine: Elsevier, (2017), pp. 239-49. e4.
5- Kazue Okamoto-Mizuno and Koh Mizuno, "Effects of thermal environment on sleep and circadian rhythm." Journal of physiological anthropology, Vol. 31 (No. 1), pp. 1-9, (2012).
6- William C Orr, "Sleep and the gastrointestinal tract." Sleep: A Comprehensive Handbook, pp. 733-40, (2005).
7- Donna L Ewing, Miranda Manassei, Cassandra Gould van Praag, Andrew O Philippides, Hugo D Critchley, and Sarah N Garfinkel, "Sleep and the heart: Interoceptive differences linked to poor experiential sleep quality in anxiety and depression." Biological psychology, Vol. 127pp. 163-72, (2017).
8- Christina M Gobin, Jonathan B Banks, Ana I Fins, and Jaime L Tartar, "Poor sleep quality is associated with a negative cognitive bias and decreased sustained attention." Journal of sleep research, Vol. 24 (No. 5), pp. 535-42, (2015).
9- Nirit Soffer-Dudek, Avi Sadeh, Ronald E Dahl, and Shiran Rosenblat-Stein, "Poor sleep quality predicts deficient emotion information processing over time in early adolescence." Sleep, Vol. 34 (No. 11), pp. 1499-508, (2011).
10- William James, "The physical basis of emotion." (1994).
11- Lutz Mussgay, N Klinkenberg, and H Rüddel, "Heart beat perception in patients with depressive, somatoform, and personality disorders." Journal of Psychophysiology, Vol. 13 (No. 1), p. 27, (1999).
12- Rainer Schandry, "Heart beat perception and emotional experience." Psychophysiology, Vol. 18 (No. 4), pp. 483-88, (1981).
13- Marcus A Gray et al., "A cortical potential reflecting cardiac function." Proceedings of the National Academy of Sciences, Vol. 104 (No. 16), pp. 6818-23, (2007).
14- Lampros Perogamvros, Hyeong-Dong Park, Laurence Bayer, Aurore A Perrault, Olaf Blanke, and Sophie Schwartz, "Increased heartbeat-evoked potential during REM sleep in nightmare disorder." NeuroImage: Clinical, Vol. 22p. 101701, (2019).
15- Frederike H Petzschner, Lilian A Weber, Katharina V Wellstein, Gina Paolini, Cao Tri Do, and Klaas E Stephan, "Focus of attention modulates the heartbeat evoked potential." NeuroImage, Vol. 186pp. 595-606, (2019).
16- Olga Pollatos and Rainer Schandry, "Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat‐evoked brain potential." Psychophysiology, Vol. 41 (No. 3), pp. 476-82, (2004).
17- Janneke Terhaar, Filipa Campos Viola, Karl-Jürgen Bär, and Stefan Debener, "Heartbeat evoked potentials mirror altered body perception in depressed patients." Clinical neurophysiology, Vol. 123 (No. 10), pp. 1950-57, (2012).
18- G Dirlich, T Dietl, L Vogl, and F Strian, "Topography and morphology of heart action-related EEG potentials." Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section, Vol. 108 (No. 3), pp. 299-305, (1998).
19- André Schulz, Florian Strelzyk, Diana S Ferreira de Sá, Ewald Naumann, Claus Vögele, and Hartmut Schächinger, "Cortisol rapidly affects amplitudes of heartbeat-evoked brain potentials—Implications for the contribution of stress to an altered perception of physical sensations?" Psychoneuroendocrinology, Vol. 38 (No. 11), pp. 2686-93, (2013).
20- Sarah N Garfinkel, Claire Tiley, Stephanie O'Keeffe, Neil A Harrison, Anil K Seth, and Hugo D Critchley, "Discrepancies between dimensions of interoception in autism: Implications for emotion and anxiety." Biological psychology, Vol. 114pp. 117-26, (2016).
21- Jennifer Murphy, Rebecca Brewer, Hannah Hobson, Caroline Catmur, and Geoffrey Bird, "Is alexithymia characterised by impaired interoception? Further evidence, the importance of control variables, and the problems with the Heartbeat Counting Task." Biological psychology, Vol. 136pp. 189-97, (2018).
22- Olga Pollatos, Rainer Schandry, Dorothee P Auer, and Christian Kaufmann, "Brain structures mediating cardiovascular arousal and interoceptive awareness." Brain research, Vol. 1141pp. 178-87, (2007).
23- Julia Lechinger, Dominik Philip Johannes Heib, Walter Gruber, Manuel Schabus, and Wolfgang Klimesch, "Heartbeat‐related EEG amplitude and phase modulations from wakefulness to deep sleep: Interactions with sleep spindles and slow oscillations." Psychophysiology, Vol. 52 (No. 11), pp. 1441-50, (2015).
24- S Mazza, M Magnin, and H Bastuji, "Pain and sleep: from reaction to action." Neurophysiologie Clinique/Clinical Neurophysiology, Vol. 42 (No. 5), pp. 337-44, (2012).
25- Sarah A Immanuel et al., "Heartbeat evoked potentials during sleep and daytime behavior in children with sleep-disordered breathing." American journal of respiratory and critical care medicine, Vol. 190 (No. 10), pp. 1149-57, (2014).
26- Mario Giovanni Terzano et al., "Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep." Sleep medicine, Vol. 2 (No. 6), pp. 537-54, (2001).
27- Arnaud Delorme and Scott Makeig, "EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis." Journal of neuroscience methods, Vol. 134 (No. 1), pp. 9-21, (2004).
28- Jiapu Pan and Willis J Tompkins, "A real-time QRS detection algorithm." IEEE transactions on biomedical engineering, (No. 3), pp. 230-36, (1985).
29- JJ Pérez, E Guijarro, and JA Barcia, "Suppression of the cardiac electric field artifact from the heart action evoked potential." Medical and Biological Engineering and Computing, Vol. 43pp. 572-81, (2005).
30- G Dirlich, L Vogl, M Plaschke, and F Strian, "Cardiac field effects on the EEG." Electroencephalography and clinical neurophysiology, Vol. 102 (No. 4), pp. 307-15, (1997).
31- Olga Pollatos, Wladimir Kirsch, and Rainer Schandry, "On the relationship between interoceptive awareness, emotional experience, and brain processes." Cognitive brain research, Vol. 25 (No. 3), pp. 948-62, (2005).
32- Eric Maris and Robert Oostenveld, "Nonparametric statistical testing of EEG-and MEG-data." Journal of neuroscience methods, Vol. 164 (No. 1), pp. 177-90, (2007).
33- Hugo D Critchley, Stefan Wiens, Pia Rotshtein, Arne Öhman, and Raymond J Dolan, "Neural systems supporting interoceptive awareness." Nature neuroscience, Vol. 7 (No. 2), pp. 189-95, (2004).
34- Ralph Adolphs, Hanna Damasio, Daniel Tranel, Greg Cooper, and Antonio R Damasio, "A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping." Journal of neuroscience, Vol. 20 (No. 7), pp. 2683-90, (2000).
35- Yishul Wei et al., "I keep a close watch on this heart of mine: increased interoception in insomnia." Sleep, Vol. 39 (No. 12), pp. 2113-24, (2016).
36- Ronald C Hamdy et al., "Insomnia and mild cognitive impairment." Gerontology and Geriatric Medicine, Vol. 4p. 2333721418778421, (2018).
37- Angela Zhang, Lei Xing, James Zou, and Joseph C Wu, "Shifting machine learning for healthcare from development to deployment and from models to data." Nature Biomedical Engineering, pp. 1-16, (2022).
| Files | ||
| Issue | Vol 11 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v11i3.15877 | |
| Keywords | ||
| Cardiac Cycle Heartbeat Evoked Potential Interoception Sleep Disorder | ||
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How to Cite
1.
Seddighi B, Mohebbi M. Investigation of Heartbeat Evoked Potential (HEP) Response During Different Stages of Sleep in Sleep Disorders. Frontiers Biomed Technol. 2024;11(3):302-314.
