About this Journal Submit a Manuscript Table of Contents
Epilepsy Research and Treatment
Volume 2013 (2013), Article ID 932790, 10 pages
http://dx.doi.org/10.1155/2013/932790
Review Article

Why Are Seizures Rare in Rapid Eye Movement Sleep? Review of the Frequency of Seizures in Different Sleep Stages

1Department of Neurology, Epilepsy Service, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA
2Department of Neurology, Division of Epilepsy, EEG, and Sleep Neurology, Brigham and Women’s-Faulkner Hospital, 1153 Centre Street, Boston, MA 02130, USA

Received 14 March 2013; Accepted 16 May 2013

Academic Editor: M. Maestri

Copyright © 2013 Marcus Ng and Milena Pavlova. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Passouant, “Historical views on sleep and epilepsy,” in Sleep and Epilepsy, M. B. Sterman, Ed., pp. 1–6, Academic Press, New York, NY, USA, 1982.
  2. E. Aserinsky and N. Kleitman, “Regularly occurring periods of eye motility, and concomitant phenomena, during sleep,” Science, vol. 118, no. 3062, pp. 273–274, 1953. View at Scopus
  3. A. Mitani, K. Ito, A. E. Hallanger, B. H. Wainer, K. Kataoka, and R. W. McCarley, “Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat,” Brain Research, vol. 451, no. 1-2, pp. 397–402, 1988. View at Scopus
  4. R. W. McCarley, R. W. Greene, D. Rainnie, and C. M. Portas, “Brainstem neuromodulation and REM sleep,” Seminars in the Neurosciences, vol. 7, no. 5, pp. 341–354, 1995. View at Publisher · View at Google Scholar · View at Scopus
  5. C. S. Leonard and R. Llinás, “Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling rem sleep: an in vitro electrophysiological study,” Neuroscience, vol. 59, no. 2, pp. 309–330, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. J. I. Luebke, R. W. Greene, K. Semba, A. Kamondi, R. W. McCarley, and P. B. Reiner, “Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 2, pp. 743–747, 1992. View at Scopus
  7. M. M. Thakkar, R. E. Strecker, and R. W. McCarley, “Behavioral state control through differential serotonergic inhibition in the mesopontine cholinergic nuclei: a simultaneous unit recording and microdialysis study,” Journal of Neuroscience, vol. 18, no. 14, pp. 5490–5497, 1998. View at Scopus
  8. S. Chokroverty, “Neurobiology of rapid eye movement and non-rapid eye movement sleep,” in Sleep Disorders Medicine: Basic Science, Technical Considerations, and Clinical Aspects, S. Chokroverty, Ed., pp. 29–58, Saunders Elsevier, Philadelphia, Pa, USA, 3rd edition, 2009.
  9. M. Steriade and R. W. McCarley, Brain Control of Sleep and Wakefulness, Kluwer Academic Publishers, New York, NY, USA, 2005.
  10. R. A. España and T. E. Scammell, “Sleep neurobiology from a clinical perspective,” Sleep, vol. 34, no. 7, pp. 845–858, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Boissard, D. Gervasoni, M. H. Schmidt, B. Barbagli, P. Fort, and P. H. Luppi, “The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study,” European Journal of Neuroscience, vol. 16, no. 10, pp. 1959–1973, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Boucetta and B. E. Jones, “Activity profiles of cholinergic and intermingled gabaergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats,” Journal of Neuroscience, vol. 29, no. 14, pp. 4664–4674, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. M. El Mansari, K. Sakai, and M. Jouvet, “Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats,” Experimental Brain Research, vol. 76, no. 3, pp. 519–529, 1989. View at Scopus
  14. M. G. Lee, I. D. Manns, A. Alonso, and B. E. Jones, “Sleep-wake related discharge properties of basal forebrain neurons recorded with micropipettes in head-fixed rats,” Journal of Neurophysiology, vol. 92, no. 2, pp. 1182–1198, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Steriade, S. Datta, D. Paré, G. Oakson, and R. Curró Dossi, “Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems,” Journal of Neuroscience, vol. 10, no. 8, pp. 2541–2559, 1990. View at Scopus
  16. P. Henny and B. E. Jones, “Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons,” European Journal of Neuroscience, vol. 27, no. 3, pp. 654–670, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. I. Gritti, L. Mainville, M. Mancia, and B. E. Jones, “GABAergic and other non-cholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat,” Journal of Comparative Neurology, vol. 383, pp. 163–177, 1997.
  18. K. Ito, M. Yanagihara, H. Imon, L. Dauphin, and R. W. McCarley, “Intracellular recordings of pontine medial gigantocellular tegmental field neurons in the naturally sleeping cat: behavioral state-related activity and soma size difference in order of recruitment,” Neuroscience, vol. 114, no. 1, pp. 23–37, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Sakai, J. P. Sastre, D. Salvert, M. Touret, M. Tohyama, and M. Jouvet, “Tegmentoreticular projections with special reference to the muscular atonia during paradoxical sleep in the cat: an HRP study,” Brain Research, vol. 176, no. 2, pp. 233–254, 1979. View at Publisher · View at Google Scholar · View at Scopus
  20. D. R. Curtis, L. Hösli, G. A. R. Johnston, and I. H. Johnston, “The hyperpolarization of spinal motoneurones by glycine and related amino acids,” Experimental Brain Research, vol. 5, no. 3, pp. 235–258, 1968. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Y. Lai, T. Kodama, and J. M. Siegel, “Changes in monoamine release in the ventral horn and hypoglossal nucleus linked to pontine inhibition of muscle tone: an in vivo microdialysis study,” Journal of Neuroscience, vol. 21, no. 18, pp. 7384–7391, 2001. View at Scopus
  22. A. Jelev, S. Sood, H. Liu, P. Nolan, and R. L. Horner, “Microdialysis perfusion of 5-HT into hypoglossal motor nucleus differentially modulates genioglossus activity across natural sleep-wake states in rats,” Journal of Physiology, vol. 532, no. 2, pp. 467–481, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. J. F. Perrier and R. Delgado-Lezama, “Synaptic release of serotonin induced by stimulation of the raphe nucleus promotes plateau potentials in spinal motoneurons of the adult turtle,” Journal of Neuroscience, vol. 25, no. 35, pp. 7993–7999, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Fedirchuk and Y. Dai, “Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production,” Journal of Physiology, vol. 557, no. 2, pp. 355–361, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. S. L. Foote, G. Aston-Jones, and F. E. Bloom, “Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 5, pp. 3033–3037, 1980. View at Scopus
  26. G. Aston-Jones and F. E. Bloom, “Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle,” Journal of Neuroscience, vol. 1, no. 8, pp. 876–886, 1981. View at Scopus
  27. G. Aston-Jones and F. E. Bloom, “Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli,” Journal of Neuroscience, vol. 1, no. 8, pp. 887–900, 1981. View at Scopus
  28. J. A. Hobson, R. W. Mccarley, and P. W. Wyzinski, “Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups,” Science, vol. 189, no. 4196, pp. 55–58, 1975. View at Scopus
  29. D. J. McGinty and R. M. Harper, “Dorsal raphe neurons: depression of firing during sleep in cats,” Brain Research, vol. 101, no. 3, pp. 569–575, 1976. View at Publisher · View at Google Scholar · View at Scopus
  30. J. A. Hobson, R. W. McCarley, and J. P. Nelson, “Location and spike-train characteristics of cells in anterodorsal pons having selective decreases in firing rate during desynchronized sleep,” Journal of Neurophysiology, vol. 50, no. 4, pp. 770–783, 1983. View at Scopus
  31. K. Rasmussen, J. Heym, and B. L. Jacobs, “Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats,” Experimental Neurology, vol. 83, no. 2, pp. 302–317, 1984. View at Scopus
  32. C. Fornal, S. Auerbach, and B. L. Jacobs, “Activity of serotonin-containing neurons in nucleus raphe magnus in freely moving cats,” Experimental Neurology, vol. 88, no. 3, pp. 590–608, 1985. View at Scopus
  33. R. Cespuglio, H. Faradji, M. E. Gomez, and M. Jouvet, “Single unit recordings in the nuclei raphe dorsalis and magnus during the sleep-waking cycle of semi-chronic prepared cats,” Neuroscience Letters, vol. 24, no. 2, pp. 133–138, 1981. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Sakai, G. Vanni Mercier, and M. Jouvet, “Evidence for the presence of PS-OFF neurons in the ventromedial medulla oblongata of freely moving cats,” Experimental Brain Research, vol. 49, no. 2, pp. 311–314, 1983. View at Scopus
  35. Y. Kayama, M. Ohta, and E. Jodo, “Firing of “possibly” cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness,” Brain Research, vol. 569, no. 2, pp. 210–220, 1992. View at Publisher · View at Google Scholar · View at Scopus
  36. R. W. Mccarley and J. A. Hobson, “Neuronal excitability modulation over the sleep cycle: a structural and mathematical model,” Science, vol. 189, no. 4196, pp. 58–60, 1975. View at Scopus
  37. B. E. Jones, “The organization of central cholinergic systems and their functional importance in sleep-waking states,” Progress in Brain Research, vol. 98, pp. 61–71, 1993. View at Scopus
  38. R. Lydic, R. W. McCarley, and J. A. Hobson, “Serotonin neurons and sleep. I. Long term recordings of dorsal raphe discharge frequency and PGO waves,” Archives Italiennes de Biologie, vol. 125, no. 4, pp. 317–343, 1987. View at Scopus
  39. R. W. McCarley and S. G. Massaquoi, “A limit cycle mathematical model of the REM sleep oscillator system,” American Journal of Physiology, vol. 251, no. 6, pp. 1011–1029, 1986. View at Scopus
  40. D. Minecan, A. Natarajan, M. Marzec, and B. Malow, “Relationship of epileptic seizures to sleep stage and sleep depth,” Sleep, vol. 25, no. 8, pp. 899–904, 2002. View at Scopus
  41. A. Crespel, M. Baldy-Moulinier, and P. Coubes, “The relationship between sleep and epilepsy in frontal and temporal lobe epilepsies: practical and physiopathologic considerations,” Epilepsia, vol. 39, no. 2, pp. 150–157, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. M. G. Terzano, L. Parrino, P. G. Garofalo, C. Durisotti, and C. Filati-Roso, “Activation of partial seizures with motor signs during cyclic alternating pattern in human sleep,” Epilepsy Research, vol. 10, no. 2-3, pp. 166–173, 1991. View at Publisher · View at Google Scholar · View at Scopus
  43. S. T. Herman, T. S. Walczak, and C. W. Bazil, “Distribution of partial seizures during the sleep-wake cycle: differences by seizure onset site,” Neurology, vol. 56, no. 11, pp. 1453–1459, 2001. View at Scopus
  44. P. Halász, J. Filakovszky, A. Vargha, and G. Bagdy, “Effect of sleep deprivation on spike-wave discharges in idiopathic generalised epilepsy: a 4 × 24 h continuous long term EEG monitoring study,” Epilepsy Research, vol. 51, no. 1-2, pp. 123–132, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Parrino, A. Smerieri, and M. G. Terzano, “Combined influence of cyclic arousability and EEG synchrony on generalized interictal discharges within the sleep cycle,” Epilepsy Research, vol. 44, no. 1, pp. 7–18, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Horita, E. Uchida, and K. Maekawa, “Circadian rhythm of regular spike-wave discharges in childhood absence epilepsy,” Brain and Development, vol. 13, no. 3, pp. 200–202, 1991. View at Scopus
  47. A. Autret, B. Lucas, and F. Laffont, “Two distinct classifications of adult epilepsies: by time of seizures and by sensitivity of the interictal paroxysmal activities to sleep and waking,” Electroencephalography and Clinical Neurophysiology, vol. 66, no. 3, pp. 211–218, 1987. View at Scopus
  48. A. Autret, B. Lucas, C. Hommet, P. Corcia, and B. de Toffol, “Sleep and the epilepsies,” Journal of Neurology, vol. 244, pp. S10–S17, 1997.
  49. J. Touchon, “Effect of awakening on epileptic activity in primary generalized myoclonic epilepsy,” in Sleep and Epilepsy, M. B. Sterman, Ed., pp. 239–248, Academic Press, New York, NY, USA, 1982.
  50. P. Kellaway, J. D. Frost, and J. W. Crawley, “Time modulation of spike-and-wave activity in generalized epilepsy,” Annals of Neurology, vol. 8, no. 5, pp. 491–500, 1980. View at Scopus
  51. S. Sato, F. E. Dreifuss, and J. K. Penry, “The effect of sleep on spike wave discharges in absence seizures,” Neurology, vol. 23, no. 12, pp. 1335–1345, 1973. View at Scopus
  52. J. J. Ross, L. C. Johnson, and R. D. Walter, “Spike and wave discharges during stages of sleep.,” Archives of Neurology, vol. 14, no. 4, pp. 399–407, 1966. View at Scopus
  53. J. M. Zeitzer, C. L. Buckmaster, K. J. Parker, C. M. Hauck, D. M. Lyons, and E. Mignot, “Circadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness,” Journal of Neuroscience, vol. 23, no. 8, pp. 3555–3560, 2003. View at Scopus
  54. P. Bourgin, S. Huitron-Resendiz, A. D. Spier et al., “Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons,” Journal of Neuroscience, vol. 20, no. 20, pp. 7760–7765, 2000. View at Scopus
  55. R. E. Brown, O. Sergeeva, K. S. Eriksson, and H. L. Haas, “Orexin A excites serotonergic neurons in the dorsal raphe nucleus of the rat,” Neuropharmacology, vol. 40, no. 3, pp. 457–459, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Eggermann, M. Serafin, L. Bayer et al., “Orexins/hypocretins excite basal forebrain cholinergic neurones,” Neuroscience, vol. 108, no. 2, pp. 177–181, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. J. N. Marcus, C. J. Aschkenasi, C. E. Lee et al., “Differential expression of Orexin receptors 1 and 2 in the rat brain,” Journal of Comparative Neurology, vol. 435, no. 1, pp. 6–25, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Verret, R. Goutagny, P. Fort et al., “A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep,” BMC Neuroscience, vol. 4, article 19, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. M. N. Alam, H. Gong, T. Alam, R. Jaganath, D. McGinty, and R. Szymusiak, “Sleep-waking discharge patterns of neurons recorded in the rat perifornical lateral hypothalamic area,” Journal of Physiology, vol. 538, no. 2, pp. 619–631, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Koyama, K. Takahashi, T. Kodama, and Y. Kayama, “State-dependent activity of neurons in the perifornical hypothalamic area during sleep and waking,” Neuroscience, vol. 119, no. 4, pp. 1209–1219, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Ahnaou, W. H. I. M. Drinkenburg, J. A. Bouwknecht, J. Alcazar, T. Steckler, and F. M. Dautzenberg, “Blocking melanin-concentrating hormone MCH1 receptor affects rat sleep-wake architecture,” European Journal of Pharmacology, vol. 579, no. 1–3, pp. 177–188, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. J. T. Willie, C. M. Sinton, E. Maratos-Flier, and M. Yanagisawa, “Abnormal response of melanin-concentrating hormone deficient mice to fasting: hyperactivity and rapid eye movement sleep suppression,” Neuroscience, vol. 156, no. 4, pp. 819–829, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Billard, A. Autret, S. Markabi et al., “The influence of vigilance states on paroxysmal EEG activities and clinical seizures in children,” Electroencephalography and Clinical Neurophysiology, vol. 75, no. 3, pp. 127–135, 1990. View at Scopus
  64. B. Dalla Bernardina, S. Bondavalli, and V. Colamaria, “Benign epilepsy of childhood with rolandic spikes (BERS) during sleep,” in Sleep and Epilepsy, M. B. Sterman, Ed., pp. 239–248, Academic Press, New York, NY, USA, 1982.
  65. Z. Clemens, J. Janszky, B. Clemens, A. Szucs, and P. Halász, “Factors affecting spiking related to sleep and wake states in temporal lobe epilepsy (TLE),” Seizure, vol. 14, no. 1, pp. 52–57, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. Z. Clemens, J. Janszky, A. Szucs, M. Békésy, B. Clemens, and P. Halász, “Interictal epileptic spiking during sleep and wakefulness in mesial temporal lobe epilepsy: a comparative study of scalp and foramen ovale electrodes,” Epilepsia, vol. 44, no. 2, pp. 186–192, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. F. Ferrillo, M. Beelke, F. De Carli et al., “Sleep-EEG modulation of interictal epileptiform discharges in adult partial epilepsy: a spectral analysis study,” Clinical Neurophysiology, vol. 111, no. 5, pp. 916–923, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. B. A. Malow, X. Lin, R. Kushwaha, and M. S. Aldrich, “Interictal spiking increases with sleep depth in temporal lobe epilepsy,” Epilepsia, vol. 39, no. 12, pp. 1309–1316, 1998. View at Publisher · View at Google Scholar · View at Scopus
  69. B. A. Malow, R. Kushwaha, X. Lin, K. J. Morton, and M. S. Aldrich, “Relationship of interictal epileptiform discharges to sleep depth in partial epilepsy,” Electroencephalography and Clinical Neurophysiology, vol. 102, no. 1, pp. 20–26, 1997. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Billiard, A. Autret, F. Laffont et al., “Aphasie acquise de l’enfant avec épilepsie à propos de 4 observations avec état de mal électrique infraclinique du sommeil,” Revue d’Electroencéphalographie et de Neurophysiologie Clinique, vol. 11, pp. 457–467, 1981.
  71. G. F. Rossi, G. Colicchio, P. Pola, and R. Roselli, “Sleep and epileptic activity,” in Epilepsy, Sleep and Sleep Deprivation, R. Degen, Ed., pp. 35–46, Elsevier Science Publishers B.V., Amsterdam, The Netherlands, 1984.
  72. G. F. Rossi, G. Colicchio, and P. Pola, “Interictal epileptic activity during sleep: a stereo-EEG study in patients with partial epilepsy,” Electroencephalography and Clinical Neurophysiology, vol. 58, no. 2, pp. 97–106, 1984. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Montplaisir, M. Laverdière, and J. M. Saint-Hilaire, “Sleep and focal epilepsy: contribution of depth recording,” in Sleep and Epilepsy, M. B. Sterman, Ed., pp. 301–314, Academic Press, New York, NY, USA, 1982.
  74. M. Sammaritano, G. L. Gigli, and J. Gotman, “Interictal spiking during wakefulness and sleep and the localization of foci in temporal lobe epilepsy,” Neurology, vol. 41, no. 2, pp. 290–297, 1991. View at Scopus
  75. C. W. Bazil and T. S. Walczak, “Effects of sleep and sleep stage on epileptic and nonepileptic seizures,” Epilepsia, vol. 38, no. 1, pp. 56–62, 1997. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Sinha, M. Brady, C. A. Scott, and M. C. Walker, “Do seizures in patients with refractory epilepsy vary between wakefulness and sleep?” Journal of Neurology, Neurosurgery and Psychiatry, vol. 77, no. 9, pp. 1076–1078, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Billiard, A. Besset, Z. Zachariev, J. Touchon, M. Baldy-Moulinier, and J. Cadilhac, “Relation of seizures and seizure discharges to sleep stages,” in Advances in Epileptology, P. Wolf, Ed., pp. 665–670, Raven Press, New York, NY, USA, 1987.
  78. B. A. Malow, R. J. Bowes, and D. Ross, “Relationship of temporal lobe seizures to sleep and arousal: a combined scalp-intracranial electrode study,” Sleep, vol. 23, no. 2, pp. 231–234, 2000. View at Scopus
  79. J. Montplaisir, M. Laverdière, J. M. Saint-Hilaire, and I. Rouleau, “Nocturnal sleep recording in partial epilepsy: a study with depth electrodes,” Journal of Clinical Neurophysiology, vol. 4, no. 4, pp. 383–388, 1987. View at Scopus
  80. B. Dalla Bernardina, F. Pajno-Ferrara, and G. Beghini, “Proceedings: rolandic spike activation during sleep in children with and without epilepsy,” Electroencephalography and Clinical Neurophysiology, vol. 39, no. 5, p. 537, 1975. View at Scopus
  81. P. Genton, B. Maton, M. Ogihara et al., “Continuous focal spikes during REM sleep in a case of acquired aphasia (Landau-Kleffner syndrome),” Sleep, vol. 15, no. 5, pp. 454–460, 1992. View at Scopus
  82. C. A. Tassinari, “Electrical status epilepticus during sleep in children (ESES),” in Sleep and Epilepsy, M. B. Sterman, Ed., pp. 465–479, Academic Press, New York, NY, USA, 1982.
  83. R. A. Hrachovy, J. D. Frost, and P. Kellaway, “Sleep characteristics in infantile spasms,” Neurology, vol. 31, no. 6, pp. 688–694, 1981. View at Scopus
  84. H. G. Wieser, “Temporal lobe epilepsy, sleep and arousal: stereo-EEG findings,” in Epilepsy, Sleep and Sleep Deprivation, R. Degen, Ed., pp. 137–167, Elsevier Science Publishers B.V., Amsterdam, The Netherlands, 1984.
  85. D. W. Klass, “Electroencephalographic manifestations of complex partial seizures,” Advances in Neurology, vol. 11, pp. 113–140, 1975. View at Scopus
  86. J. R. Hughes and S. F. Olson, “An investigation of eight different types of temporal lobe discharges,” Epilepsia, vol. 22, no. 4, pp. 421–435, 1981. View at Scopus
  87. A. Ochi, R. Hung, S. Weiss et al., “Lateralized interictal epileptiform discharges during rapid eye movement sleep correlate with epileptogenic hemisphere in children with intractable epilepsy secondary to tuberous sclerosis complex,” Epilepsia, vol. 52, pp. 1986–1994, 2011.
  88. B. A. Malow and M. S. Aldrich, “Localizing value of rapid eye movement sleep in temporal lobe epilepsy,” Sleep Medicine, vol. 1, no. 1, pp. 57–60, 2000. View at Scopus
  89. J. P. Lieb, J. P. Joseph, J. Engel, J. Walker, and P. H. Crandall, “Sleep state and seizure foci related to depth spike activity in patients with temporal lobe epilepsy,” Electroencephalography and Clinical Neurophysiology, vol. 49, no. 5-6, pp. 538–557, 1980. View at Scopus
  90. M. N. Shouse, J. M. Siegel, M. F. Wu, R. Szymusiak, and A. R. Morrison, “Mechanisms of seizure suppression during rapid-eye-movement (REM) sleep in cats,” Brain Research, vol. 505, no. 2, pp. 271–282, 1989. View at Publisher · View at Google Scholar · View at Scopus
  91. M. N. Shouse, P. R. Farber, and R. J. Staba, “Physiological basis: how NREM sleep components can promote and REM sleep components can suppress seizure discharge propagation,” Clinical Neurophysiology, vol. 111, no. 2, pp. S9–S18, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. R. A. B. Badawy, A. S. Harvey, and R. A. L. Macdonell, “Cortical hyperexcitability and epileptogenesis: understanding the mechanisms of epilepsy—part 1,” Journal of Clinical Neuroscience, vol. 16, no. 3, pp. 355–365, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. C. W. Wu, P. Y. Liu, Y. C. Wu et al., “Variations in connectivity in the sensorimotor and default-mode networks during the first nocturnal sleep cycle,” Brain Connectivity, vol. 2, pp. 177–190, 2012.
  94. L. V. Colom, “Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease,” Journal of Neurochemistry, vol. 96, no. 3, pp. 609–623, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. J. W. Miller, G. M. Turner, and B. C. Gray, “Anticonvulsant effects of the experimental induction of hippocampal theta activity,” Epilepsy Research, vol. 18, no. 3, pp. 195–204, 1994. View at Publisher · View at Google Scholar · View at Scopus
  96. E. B. Bromfield, J. E. Cavazos, and J. I. Sirven, “Basic mechanisms underlying seizures and epilepsy,” in An Introduction to Epilepsy, pp. 1–30, American Epilepsy Society, West Hartford, Conn, USA, 2006.
  97. R. A. B. Badawy, A. S. Harvey, and R. A. L. Macdonell, “Cortical hyperexcitability and epileptogenesis: understanding the mechanisms of epilepsy—Part 2,” Journal of Clinical Neuroscience, vol. 16, no. 4, pp. 485–500, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. D. J. Chong and L. J. Hirsch, “Which EEG patterns warrant treatment in the critically ill? Reviewing the evidence for treatment of periodic epileptiform discharges and related patterns,” Journal of Clinical Neurophysiology, vol. 22, no. 2, pp. 79–91, 2005. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Koike, S. Kan, M. Misaki, and S. Miyauchi, “Connectivity pattern changes in default-mode network with deep non-REM and REM sleep,” Neuroscience Research, vol. 69, no. 4, pp. 322–330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. S. I. Dimitriadis, N. A. Laskaris, Y. Del Rio-Portilla, and G. C. Koudounis, “Characterizing dynamic functional connectivity across sleep stages from EEG,” Brain Topography, vol. 22, no. 2, pp. 119–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Massimini, F. Ferrarelli, M. J. Murphy et al., “Cortical reactivity and effective connectivity during REM sleep in humans,” Cognitive Neuroscience, vol. 1, no. 3, pp. 176–183, 2010. View at Publisher · View at Google Scholar · View at Scopus