Login | Register

Sleep Spindles Predict Stress-Related Increases in Sleep Disturbances

Title:

Sleep Spindles Predict Stress-Related Increases in Sleep Disturbances

Dang-Vu, Thien Thanh, Salimi, Ali, Boucetta, Soufiane, Wenzel, Kerstin, O'Byrne, Jordan, Brandewinder, Marie, Berthomier, Christian and Gouin, Jean-Philippe (2015) Sleep Spindles Predict Stress-Related Increases in Sleep Disturbances. Frontiers in Human Neuroscience, 9 . ISSN 1662-5161

[img]
Preview
Text (application/pdf)
dang-vu-frontiers-2015.pdf - Published Version
Available under License Spectrum Terms of Access.
846kB

Official URL: http://dx.doi.org/10.3389/fnhum.2015.00068

Abstract

Background and Aim: Predisposing factors place certain individuals at higher risk for insomnia, especially in the presence of precipitating conditions such as stressful life events. Sleep spindles have been shown to play an important role in the preservation of sleep continuity. Lower spindle density might thus constitute an objective predisposing factor for sleep reactivity to stress. The aim of this study was therefore to evaluate the relationship between baseline sleep spindle density and the prospective change in insomnia symptoms in response to a standardized academic stressor.

Methods: Twelve healthy students had a polysomnography recording during a period of lower stress at the beginning of the academic semester, along with an assessment of insomnia complaints using the insomnia severity index (ISI). They completed a second ISI assessment at the end of the semester, a period coinciding with the week prior to final examinations and thus higher stress. Spindle density, amplitude, duration, and frequency, as well as sigma power were computed from C4–O2 electroencephalography derivation during stages N2–N3 of non-rapid-eye-movement (NREM) sleep, across the whole night and for each NREM sleep period. To test for the relationship between spindle density and changes in insomnia symptoms in response to academic stress, spindle measurements at baseline were correlated with changes in ISI across the academic semester.

Results: Spindle density (as well as spindle amplitude and sigma power), particularly during the first NREM sleep period, negatively correlated with changes in ISI (p < 0.05).

Conclusion: Lower spindle activity, especially at the beginning of the night, prospectively predicted larger increases in insomnia symptoms in response to stress. This result indicates that individual differences in sleep spindle activity contribute to the differential vulnerability to sleep disturbances in the face of precipitating factors.

Divisions:Concordia University > Faculty of Arts and Science > Exercise Science
Item Type:Article
Refereed:Yes
Authors:Dang-Vu, Thien Thanh and Salimi, Ali and Boucetta, Soufiane and Wenzel, Kerstin and O'Byrne, Jordan and Brandewinder, Marie and Berthomier, Christian and Gouin, Jean-Philippe
Journal or Publication:Frontiers in Human Neuroscience
Date:2015
Funders:
  • Concordia Open Access Author Fund
Digital Object Identifier (DOI):10.3389/fnhum.2015.00068
ID Code:982231
Deposited By: DANIELLE DENNIE
Deposited On:17 Mar 2017 19:26
Last Modified:18 Jan 2018 17:54

References:

APA. (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Arlington, VA: American Psychiatric Publishing.

Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., et al. (2011). Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. 217, 117–121. doi:10.1016/j.bbr.2010.10.019

Bastien, C. H., St-Jean, G., Turcotte, I., Morin, C. M., Lavallee, M., and Carrier, J. (2009). Sleep spindles in chronic psychophysiological insomnia. J. Psychosom. Res. 66, 59–65. doi:10.1016/j.jpsychores.2008.05.013

Bastien, C. H., Vallieres, A., and Morin, C. M. (2001). Validation of the insomnia severity index as an outcome measure for insomnia research. Sleep Med. 2, 297–307. doi:10.1016/S1389-9457(00)00065-4

Bastien, C. H., Vallieres, A., and Morin, C. M. (2004). Precipitating factors of insomnia. Behav. Sleep Med. 2, 50–62. doi:10.1207/s15402010bsm0201_5

Bergmann, T. O., Molle, M., Diedrichs, J., Born, J., and Siebner, H. R. (2012). Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage 59, 2733–2742. doi:10.1016/j.neuroimage.2011.10.036

Berthomier, C., Drouot, X., Herman-Stoica, M., Berthomier, P., Prado, J., Bokar-Thire, D., et al. (2007). Automatic analysis of single-channel sleep EEG: validation in healthy individuals. Sleep 30, 1587–1595.

Bodizs, R., Kis, T., Lazar, A. S., Havran, L., Rigo, P., Clemens, Z., et al. (2005). Prediction of general mental ability based on neural oscillation measures of sleep. J. Sleep Res. 14, 285–292. doi:10.1111/j.1365-2869.2005.00472.x

Buysse, D. J., Reynolds, C. F. III, Monk, T. H., Berman, S. R., and Kupfer, D. J. (1989). The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 28, 193–213. doi:10.1016/0165-1781(89)90047-4

Cote, K. A., Epps, T. M., and Campbell, K. B. (2000). The role of the spindle in human information processing of high-intensity stimuli during sleep. J. Sleep Res. 9, 19–26. doi:10.1046/j.1365-2869.2000.00188.x

Dang-Vu, T. T., Bonjean, M., Schabus, M., Boly, M., Darsaud, A., Desseilles, M., et al. (2011). Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U.S.A. 108, 15438–15443. doi:10.1073/pnas.1112503108

Dang-Vu, T. T., McKinney, S. M., Buxton, O. M., Solet, J. M., and Ellenbogen, J. M. (2010). Spontaneous brain rhythms predict sleep stability in the face of noise. Curr. Biol. 20, R626–R627. doi:10.1016/j.cub.2010.06.032

De Gennaro, L., and Ferrara, M. (2003). Sleep spindles: an overview. Sleep Med. Rev. 7, 423–440. doi:10.1053/smrv.2002.0252

De Gennaro, L., Ferrara, M., and Bertini, M. (2000). Topographical distribution of spindles: variations between and within NREM sleep cycles. Sleep Res. Online 3, 155–160. doi:10.1046/j.1365-2869.2000.00193.x

De Gennaro, L., Ferrara, M., Vecchio, F., Curcio, G., and Bertini, M. (2005). An electroencephalographic fingerprint of human sleep. Neuroimage 26, 114–122. doi:10.1016/j.neuroimage.2005.01.020

Drake, C., Richardson, G., Roehrs, T., Scofield, H., and Roth, T. (2004). Vulnerability to stress-related sleep disturbance and hyperarousal. Sleep 27, 285–291.

Drake, C. L., Jefferson, C., Roehrs, T., and Roth, T. (2006). Stress-related sleep disturbance and polysomnographic response to caffeine. Sleep Med. 7, 567–572. doi:10.1016/j.sleep.2006.03.019

Drake, C. L., Pillai, V., and Roth, T. (2014). Stress and sleep reactivity: a prospective investigation of the stress-diathesis model of insomnia. Sleep 37, 1295–1304. doi:10.5665/sleep.3916

Feinberg, I., and Floyd, T. C. (1979). Systematic trends across the night in human sleep cycles. Psychophysiology 16, 283–291. doi:10.1111/j.1469-8986.1979.tb02991.x

Fernandez-Mendoza, J., Shaffer, M. L., Olavarrieta-Bernardino, S., Vgontzas, A. N., Calhoun, S. L., Bixler, E. O., et al. (2014). Cognitive-emotional hyperarousal in the offspring of parents vulnerable to insomnia: a nuclear family study. J. Sleep Res. 23, 489–498. doi:10.1111/jsr.12168

Fernandez-Mendoza, J., Vela-Bueno, A., Vgontzas, A. N., Ramos-Platon, M. J., Olavarrieta-Bernardino, S., Bixler, E. O., et al. (2010). Cognitive-emotional hyperarousal as a premorbid characteristic of individuals vulnerable to insomnia. Psychosom. Med. 72, 397–403. doi:10.1097/PSY.0b013e3181d75319

Fernandez-Mendoza, J., Vgontzas, A. N., Bixler, E. O., Singareddy, R., Shaffer, M. L., Calhoun, S. L., et al. (2012). Clinical and polysomnographic predictors of the natural history of poor sleep in the general population. Sleep 35, 689–697. doi:10.5665/sleep.1832

Fogel, S. M., Nader, R., Cote, K. A., and Smith, C. T. (2007). Sleep spindles and learning potential. Behav. Neurosci. 121, 1–10. doi:10.1037/0735-7044.121.1.1

Fogel, S. M., and Smith, C. T. (2011). The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci. Biobehav. Rev. 35, 1154–1165. doi:10.1016/j.neubiorev.2010.12.003

Gaillard, J. M., and Blois, R. (1981). Spindle density in sleep of normal subjects. Sleep 4, 385–391.

Gais, S., Molle, M., Helms, K., and Born, J. (2002). Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830–6834.

Harvey, C. J., Gehrman, P., and Espie, C. A. (2014). Who is predisposed to insomnia: a review of familial aggregation, stress-reactivity, personality and coping style. Sleep Med. Rev. 18, 237–247. doi:10.1016/j.smrv.2013.11.004

Hasson, D., Theorell, T., Bergquist, J., and Canlon, B. (2013). Acute stress induces hyperacusis in women with high levels of emotional exhaustion. PLoS ONE 8:e52945. doi:10.1371/journal.pone.0052945

Iber, C., Ancoli-Israel, S., Chesson, A. L., and Quan, S. F. (2007). The AASM Manual for the Scoring of Sleep and Associated Events. Westchester, NY: American Academy of Sleep Medicine.

Jarrin, D. C., Chen, I. Y., Ivers, H., and Morin, C. M. (2014). The role of vulnerability in stress-related insomnia, social support and coping styles on incidence and persistence of insomnia. J. Sleep Res. 23, 681–688. doi:10.1111/jsr.12172

Jernelov, S., Hoglund, C. O., Axelsson, J., Axen, J., Gronneberg, R., Grunewald, J., et al. (2009). Effects of examination stress on psychological responses, sleep and allergic symptoms in atopic and non-atopic students. Int. J. Behav. Med. 16, 305–310. doi:10.1007/s12529-008-9020-6

LeBlanc, M., Merette, C., Savard, J., Ivers, H., Baillargeon, L., and Morin, C. M. (2009). Incidence and risk factors of insomnia in a population-based sample. Sleep 32, 1027–1037.

Lopez, J., Hoffmann, R., and Armitage, R. (2010). Reduced sleep spindle activity in early-onset and elevated risk for depression. J. Am. Acad. Child Adolesc. Psychiatry 49, 934–943. doi:10.1016/j.jaac.2010.05.014

Lovibond, P. F., and Lovibond, S. H. (1995). The structure of negative emotional states: comparison of the depression anxiety stress scales (DASS) with the beck depression and anxiety inventories. Behav. Res. Ther. 33, 335–343. doi:10.1016/0005-7967(94)00075-U

Lund, H. G., Reider, B. D., Whiting, A. B., and Prichard, J. R. (2010). Sleep patterns and predictors of disturbed sleep in a large population of college students. J. Adolesc. Health 46, 124–132. doi:10.1016/j.jadohealth.2009.06.016

Martin, N., Lafortune, M., Godbout, J., Barakat, M., Robillard, R., Poirier, G., et al. (2013). Topography of age-related changes in sleep spindles. Neurobiol. Aging 34, 468–476. doi:10.1016/j.neurobiolaging.2012.05.020

McKinney, S. M., Dang-Vu, T. T., Buxton, O. M., Solet, J. M., and Ellenbogen, J. M. (2011). Covert waking brain activity reveals instantaneous sleep depth. PLoS ONE 6:e17351. doi:10.1371/journal.pone.0017351

Morin, A., Doyon, J., Dostie, V., Barakat, M., Hadj Tahar, A., Korman, M., et al. (2008). Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 31, 1149–1156.

Riemann, D., Spiegelhalder, K., Feige, B., Voderholzer, U., Berger, M., Perlis, M., et al. (2010). The hyperarousal model of insomnia: a review of the concept and its evidence. Sleep Med. Rev. 14, 19–31. doi:10.1016/j.smrv.2009.04.002

Schabus, M., Dang-Vu, T. T., Albouy, G., Balteau, E., Boly, M., Carrier, J., et al. (2007). Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U.S.A. 104, 13164–13169. doi:10.1073/pnas.0703084104

Schabus, M., Dang-Vu, T. T., Heib, D. P., Boly, M., Desseilles, M., Vandewalle, G., et al. (2012). The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front. Neurol. 3:40. doi:10.3389/fneur.2012.00040

Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klosch, G., Anderer, P., et al. (2004). Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479–1485.

Schabus, M., Hodlmoser, K., Gruber, G., Sauter, C., Anderer, P., Klosch, G., et al. (2006). Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur. J. Neurosci. 23, 1738–1746. doi:10.1111/j.1460-9568.2006.04694.x

Spielman, A. J. (1986). Assessment of insomnia. Clin. Psychol. Rev. 6, 11–25. doi:10.1016/0272-7358(86)90015-2

Steriade, M., and McCarley, R. W. (2005). Brain Control of Wakefulness and Sleep. New York, NY: Springer.

Tamaki, M., Matsuoka, T., Nittono, H., and Hori, T. (2008). Fast sleep spindle (13-15 Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31, 204–211.

Vgontzas, A. N., Bixler, E. O., Kales, A., Manfredi, R. L., and Tyson, K. (1994). Validity and clinical utility of sleep laboratory criteria for insomnia. Int. J. Neurosci. 77, 11–21. doi:10.3109/00207459408986015

Vgontzas, A. N., Fernandez-Mendoza, J., Liao, D., and Bixler, E. O. (2013). Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. Sleep Med. Rev. 17, 241–254. doi:10.1016/j.smrv.2012.09.005
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access.

Repository Staff Only: item control page

Downloads per month over past year

Back to top Back to top