Insomnia and REM sleep instability.
arousal
insomnia
polysomnography
sleep fragmentation
Journal
Journal of sleep research
ISSN: 1365-2869
Titre abrégé: J Sleep Res
Pays: England
ID NLM: 9214441
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
11
08
2023
accepted:
14
08
2023
medline:
30
11
2023
pubmed:
8
9
2023
entrez:
8
9
2023
Statut:
ppublish
Résumé
In this narrative review, we give an overview of the concept of rapid eye movement sleep instability and its reported implications in the context of insomnia. The term rapid eye movement sleep instability was coined to describe the observation of a modified rapid eye movement quality in insomnia, characterized by an increased tendency of perceiving rapid eye movement sleep as wake, a small but consistent rapid eye movement sleep reduction and an increased rapid eye movement sleep arousal index. Current research highlights relationships that are transdiagnostic in nature, corresponding to the known interaction of insomnia with many psychiatric disorders, and showing relationships to chronic stress and anxiety disorders.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e14032Informations de copyright
© 2023 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.
Références
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.), DSM-5. APA Publishing.
Aserinsky, E., & Kleitman, N. (1953). Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science, 118, 273-274.
Aston-Jones, G., & Bloom, F. E. (1981). Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. The Journal of Neuroscience, 1, 876-886.
Baglioni, C., Johann, A. F., Benz, F., Steinmetz, L., Meneo, D., Frase, L., Kuhn, M., Ohler, M., Huart, S., Speiser, N., Tuschen-Caffier, B., Riemann, D., & Feige, B. (2023). Interactions between insomnia, sleep duration and emotional processes: An ecological momentary assessment of longitudinal influences combining self-report and physiological measures. Journal of Sleep Research, e14001.
Baglioni, C., Nanovska, S., Regen, W., Spiegelhalder, K., Feige, B., Nissen, C., Reynolds, C. F., & Riemann, D. (2016). Sleep and mental disorders: A meta-analysis of polysomnographic research. Psychological Bulletin, 142, 969-990.
Baglioni, C., Regen, W., Teghen, A., Spiegelhalder, K., Feige, B., Nissen, C., & Riemann, D. (2013). Sleep changes in the disorder of insomnia: A meta-analysis of polysomnographic studies. Sleep Medicine Reviews, 18, 195-213.
Baird, B., Mota-Rolim, S. A., & Dresler, M. (2019). The cognitive neuroscience of lucid dreaming. Neuroscience and Biobehavioral Reviews, 100, 305-323.
Ballesio, A., Zagaria, A., Curti, D. G., Moran, R., Goadsby, P. J., Rosenzweig, I., & Lombardo, C. (2023). Peripheral brain-derived neurotrophic factor (BDNF) in insomnia: A systematic review and meta-analysis. Sleep Medicine Reviews, 67, 101738.
Bastien, C. H., Vallieres, A., & Morin, C. M. (2001). Validation of the insomnia severity index as an outcome measure for insomnia research. Sleep Medicine, 2, 297-307.
Benkirane, O., Delwiche, B., Mairesse, O., & Peigneux, P. (2022). Impact of sleep fragmentation on cognition and fatigue. International Journal of Environmental Research and Public Health, 19, 15485.
Benz, F., Riemann, D., Domschke, K., Spiegelhalder, K., Johann, A. F., Marshall, N. S., & Feige, B. (2023). How many hours do you sleep? A comparison of subjective and objective sleep duration measures in a sample of insomnia patients and good sleepers. Journal of Sleep Research, 32(2), e13802.
Berger, A., Koshmanova, E., Beckers, E., Sharifpour, R., Paparella, I., Campbell, I., Mortazavi, N., Balda, F., Yi, Y. J., Lamalle, L., Dricot, L., Phillips, C., Jacobs, H. I. L., Talwar, P., El Tahry, R., Sherif, S., & Vandewalle, G. (2023). Structural and functional characterization of the locus coeruleus in young and late middle-aged individuals. Front Neuroimaging, 2, 1207844.
Boissard, R., Gervasoni, D., Schmidt, M. H., Barbagli, B., Fort, P., & Luppi, P. H. (2002). The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: A combined microinjection and functional neuroanatomical study. The European Journal of Neuroscience, 16, 1959-1973.
Bonnet, M. H. (1985). Effect of sleep disruption on sleep, performance, and mood. Sleep, 8, 11-19.
Bonnet, M. H., & Arand, D. L. (2003). Clinical effects of sleep fragmentation versus sleep deprivation. Sleep Medicine Reviews, 7, 297-310.
Buysse, D. J., Reynolds 3rd, C. F., Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989). The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatric Research, 28, 193-213.
Carskadon, M. A., Brown, E. D., & Dement, W. C. (1982). Sleep fragmentation in the elderly: Relationship to daytime sleep tendency. Neurobiology of Aging, 3, 321-327.
Castelnovo, A., Ferri, R., Galbiati, A., Rossi, A., Zucconi, M., Castronovo, V., Strambi, L. F., & Manconi, M. (2021). Extreme sleep state misperception: From psychopathology to objective-subjective sleep measures. International Journal of Psychophysiology, 167, 77-85.
Chouvarda, I., Mendez, M. O., Rosso, V., Bianchi, A. M., Parrino, L., Grassi, A., Terzano, M., Maglaveras, N., & Cerutti, S. (2011). CAP sleep in insomnia: New methodological aspects for sleep microstructure analysis. Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 2011, 1495-1498.
Chouvarda, I., Mendez, M. O., Rosso, V., Bianchi, A. M., Parrino, L., Grassi, A., Terzano, M. G., Cerutti, S., & Maglaveras, N. (2012). Cyclic alternating patterns in normal sleep and insomnia: Structure and content differences. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 20, 642-652.
Conte, F., Cerasuolo, M., Fusco, G., Giganti, F., Inserra, I., Malloggi, S., Di Iorio, I., & Ficca, G. (2021). Sleep continuity, stability and organization in good and bad sleepers. Journal of Health Psychology, 26, 2131-2142.
Conte, F., Malloggi, S., De Rosa, O., Di Iorio, I., Romano, F., Giganti, F., & Ficca, G. (2023). Sleep continuity, stability and cyclic organization are impaired in insomniacs: A case-control study. International Journal of Environmental Research and Public Health, 20(2), 1240.
Dikeos, D., Wichniak, A., Ktonas, P. Y., Mikoteit, T., Crönlein, T., Eckert, A., Kopřivová, J., Ntafouli, M., Spiegelhalder, K., Hatzinger, M., Riemann, D., & Soldatos, C. (2023). The potential of biomarkers for diagnosing insomnia: Consensus statement of the WFSBP task force on sleep disorders. The World Journal of Biological Psychiatry, 1-29. https://pubmed.ncbi.nlm.nih.gov/36880792/
Dressle R.J., Riemann D., Spiegelhalder K., Frase L., Perlis M.L., Feige B. (2023): On the relationship between EEG spectral analysis and pre- sleep cognitive arousal in insomnia disorder: Towards an integrated model of cognitive and cortical arousal. Journal of Sleep Research, 32
Duman, R. S., & Monteggia, L. M. (2006). A neurotrophic model for stress-related mood disorders. Biological Psychiatry, 59, 1116-1127.
Ermis, U., Krakow, K., & Voss, U. (2010). Arousal thresholds during human tonic and phasic REM sleep. Journal of Sleep Research, 19, 400-406.
Feige, B., Al-Shajlawi, A., Nissen, C., Voderholzer, U., Hornyak, M., Spiegelhalder, K., Kloepfer, C., Perlis, M., & Riemann, D. (2008). Does REM sleep contribute to subjective wake time in primary insomnia? A comparison of polysomnographic and subjective sleep in 100 patients. Journal of Sleep Research, 17, 180-190.
Feige, B., Baglioni, C., Boehm, P., Heinrich, A., Trumm, S., Benz, F., Nissen, C., Domschke, K., Frase, L., & Riemann, D. (2021). Event-related potentials in insomnia reflect altered perception of sleep. Sleep, 44, zsab137.
Feige, B., Baglioni, C., Spiegelhalder, K., Hirscher, V., Nissen, C., & Riemann, D. (2013). The microstructure of sleep in primary insomnia: An overview and extension. International Journal of Psychophysiology, 89, 171-180.
Feige, B., Nanovska, S., Baglioni, C., Bier, B., Cabrera, L., Diemers, S., Quellmalz, M., Siegel, M., Xeni, I., Szentkiralyi, A., Doerr, J. P., & Riemann, D. (2018). Insomnia - perchance a dream? Results from a NREM/REM sleep awakening study in good sleepers and patients with insomnia. Sleep, 41, zsy032.
Finan, P. H., Quartana, P. J., & Smith, M. T. (2015). The effects of sleep continuity disruption on positive mood and sleep architecture in healthy adults. Sleep, 38, 1735-1742.
Frase, L., Feige, B., Gioia, I., Loeck, V. K., Domschke, K., Dressle, R. J., Kilian, H., Spiegelhalder, K., Schläpfer, T., & Riemann, D. (2023). No alterations in potential indirect markers of locus coeruleus-norepinephrine function in insomnia disorder. Journal of Sleep Research, 32, e13872.
Frase, L., Spiegelhalder, K., Riemann, D., & Feige, B. (2023). The importance and limitations of polysomnography in insomnia disorder - A critical appraisal. Journal of Sleep Research.
Gauld, C., & Micoulaud-Franchi, J. A. (2022). Why could sleep medicine never do without polysomnography? Journal of Sleep Research, 31, e13541.
Gillin, J. C., Smith, T. L., Irwin, M., Butters, N., Demodena, A., & Schuckit, M. (1994). Increased pressure for rapid eye movement sleep at time of hospital admission predicts relapse in nondepressed patients with primary alcoholism at 3-month follow-up. Archives of General Psychiatry, 51, 189-197.
Gökce, F., Ehring, T., Werner, G. G., & Takano, K. (2020). Misperception of sleep is associated with intrinsic motivation toward thinking about sleep. Journal of Behavior Therapy and Experimental Psychiatry, 69, 101591.
Goldstein, A. N., & Walker, M. P. (2014). The role of sleep in emotional brain function. Annual Review of Clinical Psychology, 10, 679-708.
Gong, L., Shi, M., Wang, J., Xu, R., Yu, S., Liu, D., Ding, X., Zhang, B., Zhang, X., & Xi, C. (2021). The abnormal functional connectivity in the locus coeruleus- norepinephrine system associated with anxiety symptom in chronic insomnia disorder. Frontiers in Neuroscience, 15, 678465.
Gott, J., Rak, M., Bovy, L., Peters, E., van Hooijdonk, C. F. M., Mangiaruga, A., Varatheeswaran, R., Chaabou, M., Gorman, L., Wilson, S., Weber, F., Talamini, L., Steiger, A., & Dresler, M. (2020). Sleep fragmentation and lucid dreaming. Consciousness and Cognition, 84, 102988.
Haba-Rubio, J., Ibanez, V., & Sforza, E. (2004). An alternative measure of sleep fragmentation in clinical practice: The sleep fragmentation index. Sleep Medicine, 5, 577-581.
Hayat, H., Regev, N., Matosevich, N., Sales, A., Paredes-Rodriguez, E., Krom, A. J., Bergman, L., Li, Y., Lavigne, M., Kremer, E. J., Yizhar, O., Pickering, A. E., & Nir, Y. (2020). Locus coeruleus norepinephrine activity mediates sensory-evoked awakenings from sleep. Science Advances, 6, eaaz4232.
Iacovides, S., George, K., Kamerman, P., & Baker, F. C. (2017). Sleep fragmentation hypersensitizes healthy young women to deep and superficial experimental pain. The Journal of Pain, 18, 844-854.
Jouvet, M. (1962). Recherches sur les structures nerveuses et les mécanismes responsables des différentes phases du sommeil physiologique. Archives Italiennes de Biologie, 100, 125-206.
Kjaerby, C., Andersen, M., Hauglund, N., Ding, F., Wang, W., Xu, Q., Deng, S., Kang, N., Peng, S., Sun, Q., Dall, C., Jørgensen, P. K., Feng, J., Li, Y., Weikop, P., Hirase, H., & Nedergaard, M. (2020). Dynamic fluctuations of the locus coeruleus-norepinephrine system underlie sleep state transitions. bioRxiv 2020.09.01.274977.
Kjaerby, C., Andersen, M., Hauglund, N., Untiet, V., Dall, C., Sigurdsson, B., Ding, F., Feng, J., Li, Y., Weikop, P., Hirase, H., & Nedergaard, M. (2022). Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine. Nature Neuroscience, 25, 1059-1070.
Ko, C. H., Fang, Y. W., Tsai, L. L., & Hsieh, S. (2015). The effect of experimental sleep fragmentation on error monitoring. Biological Psychology, 104, 163-172.
Koh, K., Hamada, A., Hamada, Y., Yanase, M., Sakaki, M., Someya, K., Narita, M., Kuzumaki, N., Ikegami, D., Sakai, H., Iseki, M., Inada, E., & Narita, M. (2015). Possible involvement of activated locus coeruleus-noradrenergic neurons in pain-related sleep disorders. Neuroscience Letters, 589, 200-206.
Kussé, C., Muto, V., Mascetti, L., Matarazzo, L., Foret, A., Bourdiec, A. S. L., & Maquet, P. (2010). Neuroimaging of dreaming: State of the art and limitations. International Review of Neurobiology, 92, 87-99.
Laharnar, N., Fatek, J., Zemann, M., Glos, M., Lederer, K., Suvorov, A. V., Demin, A. V., Penzel, T., & Fietze, I. (2020). A sleep intervention study comparing effects of sleep restriction and fragmentation on sleep and vigilance and the need for recovery. Physiology & Behavior, 215, 112794.
Lee, V. V., Schembri, R., Jordan, A. S., & Jackson, M. L. (2022). The independent effects of sleep deprivation and sleep fragmentation on processing of emotional information. Behavioural Brain Research, 424, 113802.
Levine, B., Roehrs, T., Stepanski, E., Zorick, F., & Roth, T. (1987). Fragmenting sleep diminishes its recuperative value. Sleep, 10, 590-599.
Li, C., Liu, Y., Yang, N., Lan, Z., Huang, S., Wu, Y., Ma, X., & Jiang, G. (2022). Functional connectivity disturbances of the locus coeruleus in chronic insomnia disorder. Nature and Science of Sleep, 14, 1341-1350.
Li, S. B., & de Lecea, L. (2022). The brake matters: Hyperexcitable arousal circuits in sleep fragmentation with age. Clinical and Translational Medicine, 12, e900.
Liao, H. I., Yoneya, M., Kidani, S., Kashino, M., & Furukawa, S. (2016). Human pupillary dilation response to deviant auditory stimuli: Effects of stimulus properties and voluntary attention. Frontiers in Neuroscience, 10, 43.
Lipinska, G., & Thomas, K. G. F. (2019). The interaction of REM fragmentation and night-time arousal modulates sleep-dependent emotional memory consolidation. Frontiers in Psychology, 10, 1766.
Luppi, P. H., & Fort, P. (2019). Neuroanatomical and neurochemical bases of vigilance states. Sleep-Wake Neurobiology and Pharmacology, 253, 35-58. Team “Physiopathologie des reseaux neuronaux responsables du cycle veille-sommeil”, INSERM, U1028, CNRS, UMR5292, Lyon Neuroscience Research Center, Lyon, France. luppi@sommeil.univ-lyon1.fr.; University Lyon 1, Lyon, France. luppi@sommeil.univ-lyon1.fr.; Team “Physiopathologie des reseaux neuronaux responsables du cycle veille-sommeil”, INSERM, U1028, CNRS, UMR5292, Lyon Neuroscience Research Center, Lyon, France.; University Lyon 1, Lyon, France.: Springer Verlag, Berlin.
Madsen, P. L., Holm, S., Vorstrup, S., Friberg, L., Lassen, N. A., & Wildschiodtz, G. (1991). Human regional cerebral blood-flow during rapid-eye-movement sleep. Journal of Cerebral Blood Flow and Metabolism, 11, 502-507.
Madsen, P. L., Schmidt, J. F., Wildschiodtz, G., Friberg, L., Holm, S., Vorstrup, S., & Lassen, N. A. (1991). Cerebral O2-metabolism and cerebral blood-flow in humans during deep and rapid-eye-movement sleep. Journal of Applied Physiology, 70, 2597-2601.
Maquet, P. (2000). Functional neuroimaging of normal human sleep by positron emission tomography. Journal of Sleep Research, 9, 207-231.
Maquet, P., Dive, D., Salmon, E., Sadzot, B., Franco, G., Poirrier, R., von Frenckell, R., & Franck, G. (1990). Cerebral glucose-utilization during sleep wake cycle in man determined by positron emission tomography and [f-18] 2-fluoro-2-deoxy-d- glucose method. Brain Research, 513, 136-143.
Meerlo, P., Sgoifo, A., & Suchecki, D. (2008). Restricted and disrupted sleep: Effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep Medicine Reviews, 12, 197-210.
Mendelson, W. B., James, S. P., Garnett, D., Sack, D. A., & Rosenthal, N. E. (1986). A psychophysiological study of insomnia. Psychiatry Research, 19, 267-284.
Mikoteit, T., Brand, S., Eckert, A., Holsboer-Trachsler, E., & Beck, J. (2019). Brain-derived neurotrophic factor is a biomarker for subjective insomnia but not objectively assessable poor sleep continuity. Journal of Psychiatric Research, 110, 103-109.
Morris, L. S., McCall, J. G., Charney, D. S., & Murrough, J. W. (2020). The role of the locus coeruleus in the generation of pathological anxiety. Brain and Neuroscience Advances, 4, 2398212820930321.
Nicassio P. M., Mendlowitz D. R., Fussell J.J., Petras L. (1985): The phenomenology of the pre-sleep state: The development of the pre-sleep arousal scale. Behaviour Research and Therapy, 23, 263-271.
Parrino, L., Milioli, G., De Paolis, F., Grassi, A., & Terzano, M. G. (2009). Paradoxical insomnia: The role of CAP and arousals in sleep misperception. Sleep Medicine, 10, 1139-1145.
Riemann, D., Baglioni, C., Bassetti, C., Bjorvatn, B., Dolenc Groselj, L., Ellis, J. G., Espie, C. A., Garcia-Borreguero, D., Gjerstad, M., Goncalves, M., Hertenstein, E., Jansson-Fröjmark, M., Jennum, P. J., Leger, D., Nissen, C., Parrino, L., Paunio, T., Pevernagie, D., Verbraecken, J., … Spiegelhalder, K. (2017). European guideline for the diagnosis and treatment of insomnia. Journal of Sleep Research, 26, 675-700.
Riemann, D., Spiegelhalder, K., Feige, B., Voderholzer, U., Berger, M., Perlis, M., & Nissen, C. (2010). The hyperarousal model of insomnia: A review of the concept and its evidence. Sleep Medicine Reviews, 14, 19-31.
Riemann, D., Spiegelhalder, K., Nissen, C., Hirscher, V., Baglioni, C., & Feige, B. (2012). REM sleep instability - a new pathway for insomnia? Pharmacopsychiatry, 45, 167-176.
Roehrs, T., Merlotti, L., Petrucelli, N., Stepanski, E., & Roth, T. (1994). Experimental sleep fragmentation. Sleep, 17, 438-443.
Saline, A., Goparaju, B., & Bianchi, M. T. (2016). Sleep fragmentation does not explain misperception of latency or total sleep time. Journal of Clinical Sleep Medicine, 12, 1245-1255.
Sanford, L. D., Suchecki, D., & Meerlo, P. (2015). Stress, arousal, and sleep. Current Topics in Behavioral Neurosciences, 25, 379-410.
Schmitt, K., Holsboer-Trachsler, E., & Eckert, A. (2016). BDNF in sleep, insomnia, and sleep deprivation. Annals of Medicine, 48, 42-51.
Schredl, M. (2010). Characteristics and contents of dreams. International Review of Neurobiology, 92, 135-154.
Scullin, M. K., & Bliwise, D. L. (2015). Sleep, cognition, and normal aging: Integrating a half century of multidisciplinary research. Perspectives on Psychological Science, 10, 97-137.
Song, A. H., Kucyi, A., Napadow, V., Brown, E. N., Loggia, M. L., & Akeju, O. (2017). Pharmacological modulation of noradrenergic arousal circuitry disrupts functional connectivity of the locus ceruleus in humans. The Journal of Neuroscience, 37, 6938-6945.
Stepanski, E., Lamphere, J., Badia, P., Zorick, F., & Roth, T. (1984). Sleep fragmentation and daytime sleepiness. Sleep, 7, 18-26.
Sutton, B. C., & Opp, M. R. (2014). Sleep fragmentation exacerbates mechanical hypersensitivity and alters subsequent sleep-wake behavior in a mouse model of musculoskeletal sensitization. Sleep, 37, 515-524.
Tan, S., & Fan, J. (2023). A systematic review of new empirical data on lucid dream induction techniques. Journal of Sleep Research, 32, e13786.
Tang, N. K. Y., Banks, P. D. W., & Sanborn, A. N. (2023). Judgement of sleep quality of the previous night changes as the day unfolds: A prospective experience sampling study. Journal of Sleep Research, 32, e13764.
Terzano, M. G., Mancia, D., Salati, M. R., Costani, G., Decembrino, A., & Parrino, L. (1985). The cyclic alternating pattern as a physiologic component of normal NREM sleep. Sleep, 8, 137-145.
Terzano, M. G., Parrino, L., Sherieri, A., Chervin, R., Chokroverty, S., Guilleminault, C., Hirshkowitz, M., Mahowald, M., Moldofsky, H., Rosa, A., Thomas, R., & Walters, A. (2001). Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. Sleep Medicine, 2, 537-553.
Van Someren, E. J. (2021). Brain mechanisms of insomnia: New perspectives on causes and consequences. Physiological Reviews, 101, 995-1046.
Voss, U., Holzmann, R., Tuin, I., & Hobson, J. A. (2009). Lucid dreaming: A state of consciousness with features of both waking and non-lucid dreaming. Sleep, 32, 1191-1200.
Wassing, R., Benjamins, J. S., Dekker, K., Moens, S., Spiegelhalder, K., Feige, B., Riemann, D., van der Sluis, S., Van Der Werf, Y. D., Talamini, L. M., Walker, M. P., Schalkwijk, F., & Van Someren, E. J. W. (2016). Slow dissolving of emotional distress contributes to hyperarousal. Proceedings of the National Academy of Sciences, 113, 2538-2543.
Wassing, R., Benjamins, J. S., Talamini, L. M., Schalkwijk, F., & Van Someren, E. J. W. (2019). Overnight worsening of emotional distress indicates maladaptive sleep in insomnia. Sleep, 42, zsy268.
Wassing, R., Lakbila-Kamal, O., Ramautar, J. R., Stoffers, D., Schalkwijk, F., & Van Someren, E. J. W. (2019). Restless REM sleep impedes overnight amygdala adaptation. Current Biology, 29, 2351-2358.e4.
Wei, Y., Colombo, M. A., Ramautar, J. R., Blanken, T. F., van der Werf, Y. D., Spiegelhalder, K., Feige, B., Riemann, D., & Van Someren, E. J. (2017). Sleep stage transition dynamics reveal specific stage 2 vulnerability in insomnia. Sleep, 40, zsx117.
Wesensten, N. J., Balkin, T. J., & Belenky, G. L. (1999). Does sleep fragmentation impact recuperation? A review and reanalysis. Journal of Sleep Research, 8, 237-245.
Zhang, S., Hu, S., Chao, H. H., & Li, C. S. R. (2016). Resting-state functional connectivity of the locus coeruleus in humans: In comparison with the ventral tegmental area/substantia nigra pars compacta and the effects of age. Cerebral Cortex, 26, 3413-3427.