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07-03-2024 | Insomnia | Neurology • Original Article

Insomnia disorder characterized by probabilistic metastable substates using blood-oxygenation-level-dependent (BOLD) phase signals

Authors: Suzhou Wu, Huaiping Peng, Haobing Deng, Zhiwei Guo, Zhijun Jiang, Qiwen Mu

Published in: Sleep and Breathing

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Abstract

Purpose

From a clinical point of view, how to force a transition from insomnia brain state to healthy brain state by external driven stimulation is of great interest. This needs to define brain state of insomnia disorder as metastable substates. The current study was to identify recurrent substates of insomnia disorder in terms of probability of occurrence, lifetime, and alternation profiles by using leading eigenvector dynamics analysis (LEiDA) method.

Methods

We enrolled 32 patients with insomnia disorder and 30 healthy subjects. We firstly obtained the BOLD phase coherence matrix from Hilbert transform of BOLD signals and then extracted all the leading eigenvectors from the BOLD phase coherence matrix for all subjects across all time points. Lastly, we clustered the leading eigenvectors using a k-means clustering algorithm to find the probabilistic metastable substates (PMS) and calculate the probability of occurrence and associated lifetime for substates.

Results

The resulting 3 clusters were optimal for brain state of insomnia disorder and healthy brain state, respectively. The occurred probabilities of the PMS were significantly different between the patients with insomnia disorder and healthy subjects, with 0.51 versus 0.44 for PMS-1 (p < 0.001), 0.25 versus 0.27 for PMS-2 (p = 0.051), and 0.24 versus 0.29 for PMS-3 (p < 0.001), as well as the lifetime (in TR) of 36.65 versus 33.15 for PMS-1 (p = 0.068), 14.36 versus 15.43 for PMS-2 (p = 0.117), and 14.80 versus 16.34 for PMS-3 (p = 0.042). The values of the diagonal of the transition matrix were much higher than the probabilities of switching states, indicating the metastable nature of substates.

Conclusion

The resulted probabilistic metastable substates hint the characteristic brain dynamics of insomnia disorder. The results may lay a foundation to help determine how to force a transition from insomnia brain state to healthy brain state by external driven stimulation.
Literature
1.
go back to reference Association AP (2013) Diagnostic and statistical manual of mental disorders, fifth edition. American Psychiatric PublishingCrossRef Association AP (2013) Diagnostic and statistical manual of mental disorders, fifth edition. American Psychiatric PublishingCrossRef
2.
go back to reference Medicine AAOS (2014) International classification of sleep disorders, 3rd ed. American Academy of Sleep Medicine Medicine AAOS (2014) International classification of sleep disorders, 3rd ed. American Academy of Sleep Medicine
3.
go back to reference Meir Kryger TR, William C (2017) Dement, Principles and practice of sleep medicine, 6th edition. Elsevier Meir Kryger TR, William C (2017) Dement, Principles and practice of sleep medicine, 6th edition. Elsevier
4.
go back to reference Spiegelhalder K, Regen W, Baglioni C, Nissen C, Riemann D, Kyle SD (2015) Neuroimaging insights into insomnia. Curr Neurol Neurosci Rep 15:9CrossRefPubMed Spiegelhalder K, Regen W, Baglioni C, Nissen C, Riemann D, Kyle SD (2015) Neuroimaging insights into insomnia. Curr Neurol Neurosci Rep 15:9CrossRefPubMed
5.
go back to reference Kringelbach ML, Deco G (2020) Brain states and transitions: insights from computational neuroscience. Cell Rep 32:108128CrossRefPubMed Kringelbach ML, Deco G (2020) Brain states and transitions: insights from computational neuroscience. Cell Rep 32:108128CrossRefPubMed
6.
go back to reference Tognoli E, Kelso JA (2009) Brain coordination dynamics: true and false faces of phase synchrony and metastability. Prog Neurobiol 87:31–40CrossRefPubMed Tognoli E, Kelso JA (2009) Brain coordination dynamics: true and false faces of phase synchrony and metastability. Prog Neurobiol 87:31–40CrossRefPubMed
7.
go back to reference Michel CM, Koenig T (2018) EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: a review. Neuroimage 180:577–593CrossRefPubMed Michel CM, Koenig T (2018) EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: a review. Neuroimage 180:577–593CrossRefPubMed
8.
go back to reference Hancock F, Cabral J, Luppi AI, Rosas FE, Mediano PAM, Dipasquale O et al (2022) Metastability, fractal scaling, and synergistic information processing: what phase relationships reveal about intrinsic brain activity. Neuroimage 259:119433CrossRefPubMed Hancock F, Cabral J, Luppi AI, Rosas FE, Mediano PAM, Dipasquale O et al (2022) Metastability, fractal scaling, and synergistic information processing: what phase relationships reveal about intrinsic brain activity. Neuroimage 259:119433CrossRefPubMed
9.
go back to reference Capouskova K, Kringelbach ML, Deco G (2022) Modes of cognition: evidence from metastable brain dynamics. Neuroimage 260:119489CrossRefPubMed Capouskova K, Kringelbach ML, Deco G (2022) Modes of cognition: evidence from metastable brain dynamics. Neuroimage 260:119489CrossRefPubMed
10.
go back to reference Figueroa CA, Cabral J, Mocking RJT, Rapuano KM, van Hartevelt TJ, Deco G et al (2019) Altered ability to access a clinically relevant control network in patients remitted from major depressive disorder. Hum Brain Mapp 40:2771–2786CrossRefPubMedPubMedCentral Figueroa CA, Cabral J, Mocking RJT, Rapuano KM, van Hartevelt TJ, Deco G et al (2019) Altered ability to access a clinically relevant control network in patients remitted from major depressive disorder. Hum Brain Mapp 40:2771–2786CrossRefPubMedPubMedCentral
11.
go back to reference Kringelbach ML, Cruzat J, Cabral J, Knudsen GM, Carhart-Harris R, Whybrow PC et al (2020) Dynamic coupling of whole-brain neuronal and neurotransmitter systems. Proc Natl Acad Sci USA 117:9566–9576ADSCrossRefPubMedPubMedCentral Kringelbach ML, Cruzat J, Cabral J, Knudsen GM, Carhart-Harris R, Whybrow PC et al (2020) Dynamic coupling of whole-brain neuronal and neurotransmitter systems. Proc Natl Acad Sci USA 117:9566–9576ADSCrossRefPubMedPubMedCentral
12.
go back to reference Lord LD, Expert P, Atasoy S, Roseman L, Rapuano K, Lambiotte R et al (2019) Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin. Neuroimage 199:127–142CrossRefPubMed Lord LD, Expert P, Atasoy S, Roseman L, Rapuano K, Lambiotte R et al (2019) Dynamical exploration of the repertoire of brain networks at rest is modulated by psilocybin. Neuroimage 199:127–142CrossRefPubMed
13.
go back to reference Deco G, Cruzat J, Cabral J, Tagliazucchi E, Laufs H, Logothetis NK et al (2019) Awakening: predicting external stimulation to force transitions between different brain states. Proc Natl Acad Sci USA 116:18088–18097ADSCrossRefPubMedPubMedCentral Deco G, Cruzat J, Cabral J, Tagliazucchi E, Laufs H, Logothetis NK et al (2019) Awakening: predicting external stimulation to force transitions between different brain states. Proc Natl Acad Sci USA 116:18088–18097ADSCrossRefPubMedPubMedCentral
14.
go back to reference Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14:339–351CrossRefPubMed Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14:339–351CrossRefPubMed
16.
go back to reference Jiang B, He D, Guo Z, Gao Z (2020) Effect-size seed-based d mapping of resting-state fMRI for persistent insomnia disorder. Sleep Breath 24:653–659CrossRefPubMed Jiang B, He D, Guo Z, Gao Z (2020) Effect-size seed-based d mapping of resting-state fMRI for persistent insomnia disorder. Sleep Breath 24:653–659CrossRefPubMed
17.
go back to reference Tahmasian M, Noori K, Samea F, Zarei M, Spiegelhalder K, Eickhoff SB et al (2018) A lack of consistent brain alterations in insomnia disorder: an activation likelihood estimation meta-analysis. Sleep Med Rev 42:111–118CrossRefPubMedPubMedCentral Tahmasian M, Noori K, Samea F, Zarei M, Spiegelhalder K, Eickhoff SB et al (2018) A lack of consistent brain alterations in insomnia disorder: an activation likelihood estimation meta-analysis. Sleep Med Rev 42:111–118CrossRefPubMedPubMedCentral
19.
go back to reference Vohryzek J, Deco G, Cessac B, Kringelbach ML, Cabral J (2020) Ghost attractors in spontaneous brain activity: recurrent excursions into functionally-relevant BOLD phase-locking states. Front Syst Neurosci 14:20CrossRefPubMedPubMedCentral Vohryzek J, Deco G, Cessac B, Kringelbach ML, Cabral J (2020) Ghost attractors in spontaneous brain activity: recurrent excursions into functionally-relevant BOLD phase-locking states. Front Syst Neurosci 14:20CrossRefPubMedPubMedCentral
20.
go back to reference Fasano MC, Cabral J, Stevner A, Vuust P, Cantou P, Brattico E et al (2023) The early adolescent brain on music: analysis of functional dynamics reveals engagement of orbitofrontal cortex reward system. Hum Brain Mapp 44:429–446 Fasano MC, Cabral J, Stevner A, Vuust P, Cantou P, Brattico E et al (2023) The early adolescent brain on music: analysis of functional dynamics reveals engagement of orbitofrontal cortex reward system. Hum Brain Mapp 44:429–446
21.
go back to reference Zhou B, Wu X, Tang L, Li C (2022) Dynamics of the brain functional network associated with subjective cognitive decline and its relationship to apolipoprotein E €4 alleles. Front Aging Neurosci 14:806032CrossRefPubMedPubMedCentral Zhou B, Wu X, Tang L, Li C (2022) Dynamics of the brain functional network associated with subjective cognitive decline and its relationship to apolipoprotein E €4 alleles. Front Aging Neurosci 14:806032CrossRefPubMedPubMedCentral
22.
go back to reference Alonso Martínez S, Deco G, Ter Horst GJ, Cabral J (2020) The dynamics of functional brain networks associated with depressive symptoms in a nonclinical sample. Front Neural Circuits 14:570583CrossRefPubMedPubMedCentral Alonso Martínez S, Deco G, Ter Horst GJ, Cabral J (2020) The dynamics of functional brain networks associated with depressive symptoms in a nonclinical sample. Front Neural Circuits 14:570583CrossRefPubMedPubMedCentral
23.
go back to reference Farinha M, Amado C, Morgado P, Cabral J (2022) Increased excursions to functional networks in schizophrenia in the absence of task. Front Neurosci 16:821179CrossRefPubMedPubMedCentral Farinha M, Amado C, Morgado P, Cabral J (2022) Increased excursions to functional networks in schizophrenia in the absence of task. Front Neurosci 16:821179CrossRefPubMedPubMedCentral
24.
go back to reference Tagliazucchi E, Laufs H (2014) Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82:695–708CrossRefPubMed Tagliazucchi E, Laufs H (2014) Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82:695–708CrossRefPubMed
25.
go back to reference Altmann A, Schroter MS, Spoormaker VI, Kiem SA, Jordan D, Ilg R et al (2016) Validation of non-REM sleep stage decoding from resting state fMRI using linear support vector machines. Neuroimage 125:544–555CrossRefPubMed Altmann A, Schroter MS, Spoormaker VI, Kiem SA, Jordan D, Ilg R et al (2016) Validation of non-REM sleep stage decoding from resting state fMRI using linear support vector machines. Neuroimage 125:544–555CrossRefPubMed
Metadata
Title
Insomnia disorder characterized by probabilistic metastable substates using blood-oxygenation-level-dependent (BOLD) phase signals
Authors
Suzhou Wu
Huaiping Peng
Haobing Deng
Zhiwei Guo
Zhijun Jiang
Qiwen Mu
Publication date
07-03-2024
Publisher
Springer International Publishing
Keyword
Insomnia
Published in
Sleep and Breathing
Print ISSN: 1520-9512
Electronic ISSN: 1522-1709
DOI
https://doi.org/10.1007/s11325-024-03018-z
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