Recognition of Spontaneous and Evoked Arousal- and Sleep-Like (Antiarousal) Phasic Events

  • Péter Halász
  • Róbert Bódizs


In this chapter, we will deal with data accumulated about the arousal-driven spontaneous and evoked phasic events. We are looking for characteristics of spontaneous and elicited phasic changes, regularities in their occurrence, and the impact of their existence on the course of sleep. Summarizing the results of earlier works about PAT, K-complexes, and CAP phenomena, a new approach has been used in their systematization. First, we have differentiated arousal-like and sleep-like spontaneous and elicited responses and investigated the relation of these two types with dynamic changes in the course of night sleep. We differentiated these phasic changes from tonic states of sleep and analyzed the interrelationships of the phasic and tonic changes.


Phases d’activation transitoire K-complexes Micro-arousals Reactive delta waves Cyclic alternating pattern 


  1. Ackner B, Pampiglione G. Some relationships between peripheral vasomotor and E.E.G. changes. J Neurol Neurosurg Psychiatry. 1957;20(1):58–64.PubMedCrossRefGoogle Scholar
  2. Amzica F, Steriade M. The K-complex: its slow (<1-Hz) rhythmicity and relation to delta waves. Neurology. 1997;49(4):952–9.PubMedCrossRefGoogle Scholar
  3. ASDA (American Sleep Disorders Association). EEG arousals: scoring rules and examples. Sleep. 1992;15:173–84.Google Scholar
  4. Bastien C, Campbell K. The evoked K-complex: all-or-none phenomenon? Sleep. 1992;15(3):236–45.PubMedGoogle Scholar
  5. Bastien C, Campbell K. Effects of rate of tone-pip stimulation on the evoked K-complex. J Sleep Res. 1994;3(2):65–72.PubMedCrossRefGoogle Scholar
  6. Bastien CH, Crowley KE, Colrain IM. Evoked potential components unique to non-REM sleep: relationship to evoked K-complexes and vertex sharp waves. Int J Psychophysiol. 2002;46(3):257–74.PubMedCrossRefGoogle Scholar
  7. Bastuji H, García-Larrea L, Franc C, Mauguière F. Brain processing of stimulus deviance during slow-wave and paradoxical sleep: a study of human auditory evoked responses using the oddball paradigm. J Clin Neurophysiol. 1995;12(2):155–67.PubMedCrossRefGoogle Scholar
  8. Blake H, Gerard RW. Brain potentials during sleep. Am J Physiol. 1937;119:692–703.Google Scholar
  9. Cajochen C, Foy R, Dijk DJ. Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans. Sleep Res Online. 1999;2(3):65–9.PubMedGoogle Scholar
  10. Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C, et al. The human K-complex represents an isolated cortical down-state. Science. 2009;324(5930):1084–7.PubMedCrossRefGoogle Scholar
  11. Colrain IM. The K-complex: a 7-decade history. Sleep. 2005;28(2):255–73.PubMedGoogle Scholar
  12. Colrain IM, Webster KE, Hirst G, Campbell KB. The roles of vertex sharp waves and K-complexes in the generation of N300 in auditory and respiratory-related evoked potentials during early stage 2 NREM sleep. Sleep. 2000;23(1):97–106.PubMedGoogle Scholar
  13. Cote KA, de Lugt DR, Langley SD, Campbell KB. Scalp topography of the auditory evoked K-complex in stage 2 and slow wave sleep. J Sleep Res. 1999;8(4):263–72.PubMedCrossRefGoogle Scholar
  14. Czisch M, Wehrle R, Stiegler A, Peters H, Andrade K, Holsboer F, Sämann PG. Acoustic oddball during NREM sleep: a combined EEG/fMRI study. PLoS One. 2009;4(8):e6749.PubMedCrossRefGoogle Scholar
  15. Davis H, Davis PA, Loomis AL, Harvey EN, Hobart G. Electrical reactions of the human brain to auditory stimulation during sleep. J Neurophysiol. 1939;2:500–14.Google Scholar
  16. De Gennaro L, Ferrara M, Bertini M. The spontaneous K-complex during stage 2 sleep: is it the ‘forerunner’ of delta waves? Neurosci Lett. 2000;291(1):41–3.PubMedCrossRefGoogle Scholar
  17. Dijk DJ, Kronauer RE. Commentary: models of sleep regulation: successes and continuing ­challenges. J Biol Rhythms. 1999;14(6):569–73.PubMedGoogle Scholar
  18. Ehrhart J, Muzet A. Frequency and duration of transitory activation phases during normal or ­disturbed sleep in man. Arch Sci Physiol (Paris). 1974;28(3):213–60.Google Scholar
  19. Ferri R, Bruni O, Miano S, Terzano MG. Topographic mapping of the spectral components of the cyclic alternating pattern (CAP). Sleep Med. 2005a;6(1):29–36.PubMedCrossRefGoogle Scholar
  20. Ferri R, Rundo F, Bruni O, Terzano MG, Stam CJ. Dynamics of the EEG slow-wave synchronization during sleep. Clin Neurophysiol. 2005b;116(12):2783–95.PubMedCrossRefGoogle Scholar
  21. Ferri R, Rundo F, Bruni O, Terzano MG, Stam CJ. Regional scalp EEG slow-wave synchronization during sleep cyclic alternating pattern A1 subtypes. Neurosci Lett. 2006a;404(3):352–7.PubMedCrossRefGoogle Scholar
  22. Ferri R, Bruni O, Miano S, Plazzi G, Spruyt K, Gozal D, et al. The time structure of the cyclic alternating pattern during sleep. Sleep. 2006b;29(5):693–9.PubMedGoogle Scholar
  23. Finelli LA, Borbély AA, Achermann P. Functional topography of the human nonREM sleep ­electroencephalogram. Eur J Neurosci. 2001;13(12):2282–90.PubMedCrossRefGoogle Scholar
  24. Fruhstorfer H. Habituation and dishabituation of the human vertex response. Electroencephalogr Clin Neurophysiol. 1971;30(4):306–12.PubMedCrossRefGoogle Scholar
  25. Gora J, Colrain IM, Trinder J. The investigation of K-complex and vertex sharp wave activity in response to mid-inspiratory occlusions and complete obstructions to breathing during NREM sleep. Sleep. 2001;24(1):81–9.PubMedGoogle Scholar
  26. Halász P. Arousals without awakening – dynamic aspect of sleep. Physiol Behav. 1993;54(4):795–802.PubMedCrossRefGoogle Scholar
  27. Halász P. K-complex, a reactive EEG graphoelement of NREM sleep: an old chap in a new ­garment. Sleep Med Rev. 2005;9(5):391–412.PubMedCrossRefGoogle Scholar
  28. Halász P, Ujszászi J. Spectral features of evoked microarousals. In: Terzano MG, Halász P, Decklerck AC, editors. Phasic events and dynamic organization of sleep. New York: Raven Press; 1991. p. 85–100.Google Scholar
  29. Halász P, Kundra O, Rajna P, Pál I, Vargha M. Micro-arousals during nocturnal sleep. Acta Physiol Acad Sci Hung. 1979;54(1):1–12.PubMedGoogle Scholar
  30. Halász P. The role of the non-specific sensory activation in sleep regulation and in the pathomecha nism of generalized epilepsy with generalized spike-wave discharge. Doctoral thesis, Hungarian Academy of Sciences, Budapest; 1982.PubMedGoogle Scholar
  31. Halász P, Pál I, Rajna P. K-complex formation of the EEG in sleep. A survey and new examinations. Acta Physiol Hung. 1985;65(1):3–35.PubMedGoogle Scholar
  32. Hirshkowitz M. Arousals and anti-arousals. Sleep Med. 2002;3(3):203–4.PubMedCrossRefGoogle Scholar
  33. Horne JA. Human sleep, sleep loss and behaviour: implications for the prefrontal cortex and ­psychiatric disorder. Br J Psychiatry. 1993;162:413–9.PubMedCrossRefGoogle Scholar
  34. Hornyak M, Cejnar M, Elam M, Matousek M, Wallin BG. Sympathetic muscle nerve activity ­during sleep in man. Brain. 1991;114(Pt 3):1281–95.PubMedCrossRefGoogle Scholar
  35. Jahnke K, von Wegner F, Morzelewski A, Borisov S, Maischein M, Steinmetz H, et al. To wake or not to wake? The two-sided nature of the human K-complex. Neuroimage. 2012;59(2):1631–8.PubMedCrossRefGoogle Scholar
  36. Johnson LC, Karpan WE. Autonomic correlates of the spontaneous K-complex. Psychophysiology. 1968;4(4):444–52.PubMedCrossRefGoogle Scholar
  37. Kohsaka S, Sakai T, Kohsaka M, Fukudac N, Ariga A. Activation of the brainstem precedes and outlasts the K-complex in humans. Neuroscience. 2012;202:243–51.PubMedCrossRefGoogle Scholar
  38. Loomis AL, Harvey EN, Hobart GA. Distribution of disturbance-patterns in the human electroencephalogram, with special reference to sleep. J Neurophysiol. 1939;2:413–30.Google Scholar
  39. MacFarlane JG, Shahal B, Mously C, Moldofsky H. Periodic K-alpha sleep EEG activity and periodic limb movements during sleep: comparisons of clinical features and sleep parameters. Sleep. 1996;19(3):200–4.PubMedGoogle Scholar
  40. Marzano C, Ferrara M, Curcio G, De Gennaro L. The effects of sleep deprivation in humans: ­topographical electroencephalogram changes in non-rapid eye movement (NREM) sleep versus REM sleep. J Sleep Res. 2010;19(2):260–8.PubMedCrossRefGoogle Scholar
  41. Moruzzi G. Active processes in the brain stem during sleep. Harvey Lect. 1963;58:233–97.PubMedGoogle Scholar
  42. Nicholas CL, Trinder J, Colrain IM. Increased production of evoked and spontaneous K-complexes following a night of fragmented sleep. Sleep. 2002;25:882–7.PubMedGoogle Scholar
  43. Niiyama Y, Fushimi M, Sekine A, Hishikawa Y. K-complex evoked in NREM sleep is ­accompanied by a slow negative potential related to cognitive process. Electroencephalogr Clin Neurophysiol. 1995;95(1):27–33.PubMedCrossRefGoogle Scholar
  44. Parrino L, Ferri R, Bruni O, Terzano MG. Cyclic alternating pattern (CAP): the marker of sleep instability. Sleep Med Rev. 2012;16:27–45.PubMedCrossRefGoogle Scholar
  45. Peszka J, Harsh J. Effect of sleep deprivation on NREM sleep ERPs and related activity at sleep onset. Int J Psychophysiol. 2002;46(3):275–86.PubMedCrossRefGoogle Scholar
  46. Quattrochi JJ, Shapiro J, Verrier RL, Hobson JA. Transient cardiorespiratory events during NREM sleep: a feline model for human microarousals. J Sleep Res. 2000;9:185–91.PubMedCrossRefGoogle Scholar
  47. Rajna P, Halász P, Kundra O, Pál I. Event-related non-specific responses (K-complexes) during sleep. Acta Med Hung. 1983;40(1):33–40.PubMedGoogle Scholar
  48. Raynal D, et al. K-alpha events in hypersomniacs and normals. Sleep Res. 1974;3:144.Google Scholar
  49. Riedner BA, Hulse BK, Murphy MJ, Ferrarelli F, Tononi G. Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. Prog Brain Res. 2011;193:201–18.PubMedCrossRefGoogle Scholar
  50. Roth M, Shaw J, Green J. The form voltage distribution and physiological significance of the K-complex. Electroencephalogr Clin Neurophysiol. 1956;8(3):385–402.PubMedCrossRefGoogle Scholar
  51. Sallinen M, Kaartinen J, Lyytinen H. Is the appearance of mismatch negativity during stage 2 sleep related to the elicitation of K-complex? Electroencephalogr Clin Neurophysiol. 1994;91(2):140–8.PubMedCrossRefGoogle Scholar
  52. Sassin JF, Johnson LC. Body motility during sleep and its relation to the K-complex. Exp Neurol. 1968;22(1):133–44.PubMedCrossRefGoogle Scholar
  53. Schieber JP, Muzet A, Ferriere PJ. Phases of spontaneous transitory activation during normal sleep in humans. Arch Sci Physiol (Paris). 1971;25(4):443–65.Google Scholar
  54. Sforza E, Jouny C, Ibanez V. Cardiac activation during arousal in humans: further evidence for hierarchy in the arousal response. Clin Neurophysiol. 2000;111(9):1611–9.PubMedCrossRefGoogle Scholar
  55. Sforza E, Juony C, Ibanez V. Time-dependent variation in cerebral and autonomic activity during periodic leg movements in sleep: implications for arousal mechanisms. Clin Neurophysiol. 2002;113(6):883–91.PubMedCrossRefGoogle Scholar
  56. Smerieri A, Parrino L, Agosti M, Ferri R, Terzano MG. Cyclic alternating pattern sequences and non-cyclic alternating pattern periods in human sleep. Clin Neurophysiol. 2007;118(10):2305–13.PubMedCrossRefGoogle Scholar
  57. Takigawa M, Uchida T, Matsumoto K. Correlation between occurrences of spontaneous K-complex and the two physiological rhythms of cardiac and respiratory cycles (author’s transl). No To Shinkei. 1980;32(2):127–33.PubMedGoogle Scholar
  58. Terzano MG, Parrino L. Origin and significance of the cyclic alternating pattern (CAP). Sleep Med Rev. 2000;4(1):101–23.PubMedCrossRefGoogle Scholar
  59. Terzano MG, Mancia D, Salati MR, Costani G, Decembrino A, Parrino L. The cyclic alternating pattern as a physiologic component of normal NREM sleep. Sleep. 1985;8(2):137–45.PubMedGoogle Scholar
  60. Terzano MG, Halász P, Declerck AC, editors. Phasic events and dynamic organization of sleep. New York: Raven Press; 1991.Google Scholar
  61. Ujszászi J, Halász P. Long latency evoked potential components in human slow wave sleep. Electroencephalogr Clin Neurophysiol. 1988;69(6):516–22.PubMedCrossRefGoogle Scholar
  62. Wauquier A, Aloe L, Declerck A. K-complexes: are they signs of arousal or sleep protective? J Sleep Res. 1995;4(3):138–43.PubMedCrossRefGoogle Scholar
  63. Wennberg R. Intracranial cortical localization of the human K-complex. Clin Neurophysiol. 2010;121(8):1176–86.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2013

Authors and Affiliations

  • Péter Halász
    • 1
  • Róbert Bódizs
    • 2
  1. 1.Institute of Experimental Medicine and Institute of NeuroscienceBudapestHungary
  2. 2.Semmelweis University Institute of Behavioral ScienceBudapestHungary

Personalised recommendations