Research article Recurring Topics

Altered Sleep Mechanisms following Traumatic Brain Injury and Relation to Waking Function

  • Received: 27 August 2015 Accepted: 14 October 2015 Published: 22 October 2015
  • Sleep difficulties are commonly reported following traumatic brain injury (TBI), but few studies have systematically examined the neurophysiological characteristics of sleep. Sleep EEG was quantified over multiple nights to examine mechanisms underlying sleep disruption in individuals who had sustained a TBI and to explore the relationship between sleep disruption and waking function. Sleep was recorded from 20 individuals with a TBI (18-64 years) and 20 age-matched controls over two uninterrupted nights, as well as during a night where auditory stimuli were delivered. All participants underwent neuropsychological testing and waking performance assessment. Compared to controls, the TBI group had subjective complaints of falling asleep, delayed sleep onset on polysomnography (PSG), less Slow Wave (< 1 Hz) and delta (1-4 Hz) EEG power in non-REM sleep, fewer spontaneous and evoked k-complexes, reduced periodicity of spontaneous k-complexes, and lower amplitude of evoked k-complexes. While for controls, the density, duration and periodicity of sleep spindles diminished with deepening of non-REM as typically observed, this pattern was disrupted in the TBI group with peak spindle presentation occurring in Stage 3 sleep. Night-to-night-stability of Stage 2 spindles was high for controls but absent for the TBI group. Greater injury severity was related to fewer evoked k-complexes and lower spindle density. Greater spindle production predicted better waking function in the TBI group. Taken together, these data demonstrate impairment in sleep regulatory and inhibitory mechanisms as factors underlying sleep complaints following a TBI. Spindle generation may be adaptive or a marker of resiliency following TBI.

    Citation: Kimberly A Cote, Catherine E Milner, Tamara A Speth. Altered Sleep Mechanisms following Traumatic Brain Injury and Relation to Waking Function[J]. AIMS Neuroscience, 2015, 2(4): 203-228. doi: 10.3934/Neuroscience.2015.4.203

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  • Sleep difficulties are commonly reported following traumatic brain injury (TBI), but few studies have systematically examined the neurophysiological characteristics of sleep. Sleep EEG was quantified over multiple nights to examine mechanisms underlying sleep disruption in individuals who had sustained a TBI and to explore the relationship between sleep disruption and waking function. Sleep was recorded from 20 individuals with a TBI (18-64 years) and 20 age-matched controls over two uninterrupted nights, as well as during a night where auditory stimuli were delivered. All participants underwent neuropsychological testing and waking performance assessment. Compared to controls, the TBI group had subjective complaints of falling asleep, delayed sleep onset on polysomnography (PSG), less Slow Wave (< 1 Hz) and delta (1-4 Hz) EEG power in non-REM sleep, fewer spontaneous and evoked k-complexes, reduced periodicity of spontaneous k-complexes, and lower amplitude of evoked k-complexes. While for controls, the density, duration and periodicity of sleep spindles diminished with deepening of non-REM as typically observed, this pattern was disrupted in the TBI group with peak spindle presentation occurring in Stage 3 sleep. Night-to-night-stability of Stage 2 spindles was high for controls but absent for the TBI group. Greater injury severity was related to fewer evoked k-complexes and lower spindle density. Greater spindle production predicted better waking function in the TBI group. Taken together, these data demonstrate impairment in sleep regulatory and inhibitory mechanisms as factors underlying sleep complaints following a TBI. Spindle generation may be adaptive or a marker of resiliency following TBI.


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    [1] Orff HJ, Ayalon L, Drummond SP (2009) Traumatic brain injury and sleep disturbance: A review of current research. J Head Trauma Rehabil 24: 155-165. doi: 10.1097/HTR.0b013e3181a0b281
    [2] Wiseman-Hakes C, Colantonio A, Gargaro J (2009) Sleep and wake disorders following traumatic brain injury: A systematic review of the literature. Critical Rev Phys Rehab Med 21: 317-374. doi: 10.1615/CritRevPhysRehabilMed.v21.i3-4.70
    [3] Ouellet MC, Beaulieu-Bonneau S, Morin CM (2015) Sleep-wake disturbances after traumatic brain injury. Lancet Neurol 14: 746-757. doi: 10.1016/S1474-4422(15)00068-X
    [4] Grossman C (1949) Sensory stimulation during sleep. observations on the EEG responses to auditory stimulation during sleep in patients with brain pathology (preliminary report). Electroencephalogr Clin Neurophysiol 1: 487-490.
    [5] Harada M, Minami R, Hattori E, et al. (1976). Sleep in brain-damaged patients an all night sleep study of 105 cases. Kumamoto Med J 29: 110-127.
    [6] Schreiber S, Barkai G, Gur-Hartman T, et al. (2008) Long-lasting sleep patterns of adult patients with minor traumatic brain injury (mTBI) and non-mTBI subjects. Sleep Med 9: 481-487. doi: 10.1016/j.sleep.2007.04.014
    [7] Ouellet MC, Morin CM (2006) Subjective and objective measures of insomnia in the context of traumatic brain injury: a preliminary study. Sleep Med 7: 486-497. doi: 10.1016/j.sleep.2006.03.017
    [8] Ponsford JL, Ziino C, Parcell DL, et al. (2012) Fatigue and sleep disturbance following traumatic brain injury--their nature, causes, and potential treatments. J Head Trauma Rehabil 27: 224-233. doi: 10.1097/HTR.0b013e31824ee1a8
    [9] Lu W, Cantor JB, Aurora RN, et al. (2015) The relationship between self-reported sleep disturbance and polysomnography in individuals with traumatic brain injury. Brain Inj 19: 1-9.
    [10] Parcell DL, Ponsford JL, Redman JR, et al. (2008) Poor sleep quality and changes in objectively recorded sleep after traumatic brain injury: a preliminary study. Arch Phys Med Rehabil 89: 843-850. doi: 10.1016/j.apmr.2007.09.057
    [11] Shekleton JA, Parcell DL, Redman JR, et al. (2010) Sleep disturbance and melatonin levels following traumatic brain injury. Neurology 74: 1732-1738. doi: 10.1212/WNL.0b013e3181e0438b
    [12] Sommerauer M, Valko PO, Werth E, et al. (2013) Excessive sleep need following traumatic brain injury: a case-control study of 36 patients. J Sleep Res 22: 634-639. doi: 10.1111/jsr.12068
    [13] Mantua J, Mahan KM, Henry OS, et al. (2015) Altered sleep composition after traumatic brain injury does not affect declarative sleep-dependent memory consolidation. Front Hum Neurosci 9: 328.
    [14] Imbach LL, Valko PO, Li T, et al. (2015) Increased sleep need and daytime sleepiness 6 months after traumatic brain injury: a prospective controlled clinical trial. Brain 138: 726-735. doi: 10.1093/brain/awu391
    [15] Parsons LC, Crosby LJ, Perlis M, et al. (1976) Longitudinal sleep EEG power spectral analysis studies in adolescents with minor head injury. J Neurotrauma 14: 549-559.
    [16] Williams BR, Lazic SE, Ogilvie RD (2008) Polysomnographic and quantitative EEG analysis of subjects with long-term insomnia complaints associated with mild traumatic brain injury. Clin Neurophysiol 119: 429-438. doi: 10.1016/j.clinph.2007.11.003
    [17] Gosselin N, Lassonde M, Petit D, et al. (2009) Sleep following sport-related concussions. Sleep Med 10: 35-46. doi: 10.1016/j.sleep.2007.11.023
    [18] Khoury S, Chouchou F, Amzica F, et al. (2013) Rapid EEG activity during sleep dominates in mild traumatic brain injury patients with acute pain. J Neurotrauma 30: 633-641. doi: 10.1089/neu.2012.2519
    [19] Arbour C, Khoury S, Lavigne GJ, et al. (2015) Are NREM sleep characteristics associated to subjective sleep complaints after mild traumatic brain injury? Sleep Med 16: 534-539.
    [20] Levin H, Kraus MF (1994) The frontal lobes and traumatic brain injury. J Neuropsychiatry Clin Neurosci 6: 443-454. doi: 10.1176/jnp.6.4.443
    [21] Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment (4th ed.). New York, NY: Oxford University Press, Inc.
    [22] Giza CC, Hovda DA (2001) The neurometabolic cascade of concussion. J Athl Train 36: 228-235.
    [23] Williamson DJG, Scott JG, Adams RL (1996) Traumatic brain injury. In: Adams RL, Parsons OA, Culbertson JL, Nixon SJ, eds. Neuropsychology for clinical practice. Washington, D.C.: American Psychological Association: 9-64.
    [24] Levenstein S, Prantera C, Varvo V, et al. (1993). Development of the perceived stress questionnaire: A new tool for psychosomatic research. J Psychosom Res 37: 19-32.
    [25] Horne J, Ostberg O (1976) A self-assessment questionnaire to determine morningness-eveningness. Int J Chronobiol 4: 97-110.
    [26] Yositake H (1978) Three characteristics patterns of subjective fatigue symptoms. Ergonomics 21: 231-233. doi: 10.1080/00140137808931718
    [27] Beck AT, Ward CH, Mendelson M, et al. (1961) An inventory for measuring depression. Arch Gen Psychiatry 4: 561-571. doi: 10.1001/archpsyc.1961.01710120031004
    [28] Beck AT, Epstein N, Brown G, et al. (1988) An inventory for measuring clinical anxiety: Psychometric properties. J Consult Clin Psychol 56: 893-897. doi: 10.1037/0022-006X.56.6.893
    [29] Wechsler D (1997) Wechsler Adult Intelligence Scale - Third Edition (WAIS-III). San Antonio, TX: Pearson.
    [30] Stuss DT, Benson DF (1986) The frontal lobes. New York, NY: Raven Press.
    [31] Delis DC, Kramer JH, Kaplan E, et al. (2000) California Verbal Learning Test-Second Edition (CVLT-II). San Antonio, TX: Pearson.
    [32] Delis DC, Kaplan E, Kramer JH (2001) Delis-Kaplan Executive Function System (D-KEFS). San Antonio, TX: Pearson.
    [33] Hammill DD, Pearson NA, Widerholdt JL (1996) Comprehensive Test of Nonverbal Intelligence (CTONI). Austin, TX: Pro-Ed.
    [34] Baddeley A, Emslie H, Nimmo-Smith I (1993) Speed and Capacity of Language Processing Test (SCOLP). San Antonio, TX: Pearson.
    [35] Watson D, Clark AC, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Person Soc Psyc 54: 1063-1070. doi: 10.1037/0022-3514.54.6.1063
    [36] Pivik RT, Broughton RJ, Coppola R, et al. (1993) Guidelines for the recording and quantitative analysis of electroencephalographic activity in research contexts. Psychophysiol 30: 547-558. doi: 10.1111/j.1469-8986.1993.tb02081.x
    [37] Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques, and scoring system for sleep stages of human subjects. Washington, D.C.:N. I. H. Publishing 204, U. S. Government Printing Office.
    [38] Cote KA, Epps T, Campbell KB (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
    [39] Cote KA, de Lugt DR, Langley SD, et al. (1999) Scalp topography of the auditory evoked K-complex in stage 2 and slow wave sleep. J Sleep Res 8: 263-274.
    [40] Bastien C, Campbell K (1992) The evoked K-complex: All-or-none phenomenon? Sleep 15: 236-245.
    [41] Bastien C, Campbell K (1994) Effects of rate of tone-pip stimulation on the evoked K-complex. J Sleep Res 3: 65-72. doi: 10.1111/j.1365-2869.1994.tb00109.x
    [42] Howell DC. Statistical methods for psychology. Boston, MA: PWS-Kent Publishing, 1992.
    [43] Dien J, Santuzzi AM (2005) Application of repeated measures ANOVA to high-density ERP datasets :a review and tutorial. In: Handy TC, ed., Event-related potentials: A methods handbook. Cambridge, MA: The MIT Press: 57-84.
    [44] Dijk DJ, Hayes B, Czeisler CA (1993) Dynamics of electroencephalographic sleep spindles and slow wave activity in men: Effect of sleep deprivation. Brain Res 626: 190-199.
    [45] McGinty D, Szymusiak R (2011) Neural control of sleep in mammals. In: Kryger MH, Roth T, Dement WC (Eds.), Principles and Practice of Sleep Medicine, 5th ed., W.C. Elsevier: 54-66.
    [46] Riemann D, Spiegelhalder K, Feige B, 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
    [47] Colrain IM (2005) The K-complex: A 7-decade history. Sleep 28: 255-273.
    [48] Liotti M, Tucker DM (1992) Right hemisphere sensitivity to arousal and depression. Brain Cog 18: 138-151. doi: 10.1016/0278-2626(92)90075-W
    [49] De Gennaro L, Ferrara M, Bertini M (2000) The spontaneous K-complex during stage 2 sleep: is it the 'forerunner' of delta waves? Neurosci Lett 291: 41-43. doi: 10.1016/S0304-3940(00)01366-5
    [50] Amzica F, Steriade M (2000) Integration of low-frequency sleep oscillations in corticothalamic networks. Acta Neurobiologiae Experimentalis 60: 229-245.
    [51] Fogel SM, Smith CT, Cote KA (2007) Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res 180: 48-61. doi: 10.1016/j.bbr.2007.02.037
    [52] Mölle M, Bergmann TO, Marshall L, et al. (2011) Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep 34: 1411-1421.
    [53] Fogel SM, Nader R, Cote KA, et al. (2007) Sleep spindles and learning potential. Behav Neurosci 121: 1-10. doi: 10.1037/0735-7044.121.1.1
    [54] Bastien CH, St-Jean G, Turcotte I, et al. (2009) Spontaneous K-complexes in chronic psychophysiological insomnia. J Psychosom Res 67: 117-125.
    [55] Bastien CH, St-Jean G, Turcotte I, et al. (2009) Sleep spindles in chronic psychophysiological insomnia. J Psychosom Res 66: 59-65. doi: 10.1016/j.jpsychores.2008.05.013
    [56] Moldofsky H (2001) Sleep and pain. Sleep Med Rev 5: 385-396. doi: 10.1053/smrv.2001.0179
    [57] Armitage R (2007) Sleep and circadian rhythms in mood disorders. Acta Psychiatrica Scandinavica 115: 104-115. doi: 10.1111/j.1600-0447.2007.00968.x
    [58] Ramsawh H, Stein MB, Mellman TA (2011) Anxiety disorders. In: Kryger MH, Roth T, Dement WC (Eds.), Principles and Practice of Sleep Medicine, 5th ed., W.C. Elsevier: 1473-1487.
    [59] Baumann CR, Werth E, Stocker R, et al. (2007) Sleep-wake disturbances 6 months after traumatic brain injury: a prospective study. Brain 130: 1873-1883. doi: 10.1093/brain/awm109
    [60] Kempf J, Werth E, Kaiser PR, et al. (2010) Sleep-wake disturbances 3 years after traumatic brain injury. J Neurol Neurosurg Psychiatry 81: 1402-1405. doi: 10.1136/jnnp.2009.201913
    [61] Mahmood O, Rapport LJ, Hanks Robin A, et al. (2004) Neuropsychological performance and sleep disturbance following traumatic brain injury. J Head Trauma Rehab 19: 378-390. doi: 10.1097/00001199-200409000-00003
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