Chronobiology of epilepsy: Diagnostic and therapeutic implications of chrono-epileptology

Journal of Clinical Neurophysiology

Volumn 28, Issue 2, 2011, Pages 146-153

  Loddenkemper, Tobias ^a   Lockley, Steven W ^b,c   Kaleyias, Joseph ^a,d   Kothare, Sanjeev V ^a,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY HOSPITAL OF PATRAS   (Greece)

Author keywords

Chronobiology; Circadian patterns; Epilepsy; Epilepsy monitoring; Seizures

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE; ADENOSINE KINASE INHIBITOR; ADENOSINE RECEPTOR STIMULATING AGENT; ANTICONVULSIVE AGENT; CHRNA2 PROTEIN; CORTICOTROPIN; HYDROCORTISONE; MELATONIN; METHYLXANTHINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4; NICOTINIC RECEPTOR BETA2; SEROTONIN; THEOPHYLLINE; UNCLASSIFIED DRUG; VALPROIC ACID;

ATONIC SEIZURE; BRAIN DEPTH STIMULATION; CHRONOBIOLOGY; CHRONOPHARMACOLOGY; CHRONOTHERAPY; CIRCADIAN RHYTHM; CORTICAL DYSPLASIA; DOPAMINERGIC ACTIVITY; DOSAGE SCHEDULE COMPARISON; DRUG DELIVERY SYSTEM; DRUG MEGADOSE; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EMBRYOTOXICITY; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTIC STATE; EVENING DOSAGE; GELASTIC SEIZURE; GENETIC REGULATION; GRAND MAL SEIZURE; HOMEOSTASIS; HUMAN; HYDROCORTISONE BLOOD LEVEL; LENNOX GASTAUT SYNDROME; MATHEMATICAL MODEL; MYOCLONUS SEIZURE; NOCTURNAL SEIZURE; NONHUMAN; NONREM SLEEP; OSCILLATION; PATHOPHYSIOLOGY; PHOTOTHERAPY; PREDICTION; REM SLEEP; REVIEW; SEIZURE; SEIZURE SUSCEPTIBILITY; SLEEP DEPRIVATION; SLEEP PATTERN; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; SPIKE WAVE; SUPRACHIASMATIC NUCLEUS; TEMPORAL LOBE EPILEPSY; THALAMOCORTICAL TRACT; TONIC CLONIC SEIZURE; VAGUS NERVE STIMULATION;

BRAIN; BRAIN WAVES; CIRCADIAN RHYTHM; ELECTROENCEPHALOGRAPHY; EPILEPSY; HOMEOSTASIS; HUMANS; MOTOR ACTIVITY; NEURAL PATHWAYS; PREDICTIVE VALUE OF TESTS; SLEEP; SLEEP DISORDERS;

EID: 79955075899     PISSN: 07360258     EISSN: 15371603     Source Type: Journal    
DOI: 10.1097/WNP.0b013e31821213d4     Document Type: Review

References (100)

1. Abe M, Herzog ED, Yamazaki S, et al. Circadian rhythms in isolated brain regions. J Neurosci. 2002;22:350-356. (Pubitemid 34033512)
2. Badawy RA, Macdonell RA, Jackson GD, Berkovic SF. Why do seizures in generalized epilepsy often occur in the morning? Neurology. 2009;73:218-222.
3. Baram TZ, Mitchell WG, Brunson K, Haden E. Infantile spasms: hypothesis-driven therapy and pilot human infant experiments using corticotropin-releasing hormone receptor antagonists. Dev Neurosci. 1999;21:281-289.
4. Baxendale S. Seeing the light? Seizures and sunlight. Epilepsy Res. 2009;84: 72-76.
5. Bazil CW, Castro LH, Walczak TS. Reduction of rapid eye movement sleep by diurnal and nocturnal seizures in temporal lobe epilepsy. Arch Neurol. 2000;57:363-368. (Pubitemid 30140523)
6. Bazil CW, Walczak TS. Effects of sleep and sleep stage on epileptic and nonepileptic seizures. Epilepsia. 1997;38:56-62. (Pubitemid 27057481)
7. Bazil CW, Walzak TS. Anticonvulsants and seizures independently reduce REM sleep in patients with temporal lobe epilepsy. Epilepsia. 1998;39(suppl 6):69 (abstract).
8. Beenhakker MP, Huguenard JR. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron. 2009;62: 612-632.
9. Beersma DG. Models of human sleep regulation. Sleep Med Rev. 1998;2:31-43. (Pubitemid 128647236)
10. Bell-Pedersen D, Cassone VM, Earnest DJ, et al. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet. 2005;6:544-556. (Pubitemid 40910431)
11. Boison D. The adenosine kinase hypothesis of epileptogenesis. Prog Neurobiol. 2008;84:249-262.
12. Boison D. Methylxanthines, seizures, and excitotoxicity. Handb Exp Pharmacol. 2011;200:251-266.
13. Boison D, Stewart KA. Therapeutic epilepsy research: from pharmacological rationale to focal adenosine augmentation. Biochem Pharmacol. 2009;78: 1428-1437.
14. Borbely AA. A two process model of sleep regulation. Hum Neurobiol. 1982;1: 195-204. (Pubitemid 13213853)
15. Borbely AA, Wirz-Justice A. Sleep, sleep deprivation and depression. A hypothesis derived from a model of sleep regulation. Hum Neurobiol. 1982;1:205-210. (Pubitemid 13213854)
16. Burioka N, Fukuoka Y, Koyanagi S, et al. Asthma: chronopharmacotherapy and the molecular clock. Adv Drug Deliv Rev. 2010;62:946-955.
17. Carter ME, Adamantidis A, Ohtsu H, et al. Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions. J Neurosci. 2009;29:10939-10949.
18. Carter ME, Yizhar O, Chikahisa S, et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci. 2010;13:1526-1533.
19. Clinical Trial of Light Therapy for Epilepsy. Available at: http://clinicaltrials.gov/ct2/show/NCT01028456. Accessed November 4, 2010.
20. Cortesi F, Giannotti F, Ottaviano S. Sleep problems and daytime behavior in childhood idiopathic epilepsy. Epilepsia. 1999;40:1557-1565. (Pubitemid 29518085)
21. Crespel A, Baldy-Moulinier M, Coubes P. The relationship between sleep and epilepsy in frontal and temporal lobe epilepsies: practical and physiopathologic considerations. Epilepsia. 1998;39:150-157. (Pubitemid 28074350)
22. Czeisler CA, Weitzman E, Moore-Ede MC, et al. Human sleep: its duration and organization depend on its circadian phase. Science. 1980;210:1264-1267. (Pubitemid 11178016)
23. Dacey DM, Liao HW, Peterson BB, et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005;433:749-754. (Pubitemid 40292984)
24. Degen R. A study of the diagnostic value of waking and sleep EEGs after sleep deprivation in epileptic patients on anticonvulsive therapy. Electroencephalogr Clin Neurophysiol. 1980;49:577-584. (Pubitemid 10011284)
25. Dijk DJ, Czeisler CA. Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans. Neurosci Lett. 1994;166:63-68. (Pubitemid 24047900)
26. Dijk DJ, Czeisler CA. Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci. 1995;15:3526-3538.
27. Dijk DJ, Lockley SW. Integration of human sleep-wake regulation and circadian rhythmicity. J Appl Physiol. 2002;92:852-862. (Pubitemid 34671057)
28. Dijk DJ, Shanahan TL, Duffy JF, et al. Variation of electroencephalographic activity during non-rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans. J Physiol. 1997;505(Pt 3):851-858. (Pubitemid 28022381)
29. Dionisio J, Tatum WO 4th. Triggers and techniques in termination of partial seizures. Epilepsy Behav. 2010;17:210-214.
30. Durazzo TS, Spencer SS, Duckrow RB, et al. Temporal distributions of seizure occurrence from various epileptogenic regions. Neurology. 2008;70:1265-1271. (Pubitemid 351520950)
31. Eisensehr I, Parrino L, Noachtar S, et al. Sleep in Lennox-Gastaut syndrome: the role of the cyclic alternating pattern (CAP) in the gate control of clinical seizures and generalized polyspikes. Epilepsy Res. 2001;46:241-250. (Pubitemid 32772813)
32. Eksioglu Y, Tas E, Takeoka M, et al. Clinical presentation and acute treatment of electrical status epilepticus in sleep and sleep potentiated spikes. Neurology. 2010;A434 (abstract).
33. Frucht MM, Quigg M, Schwaner C, Fountain NB. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia. 2000;41:1534-1539. (Pubitemid 32002725)
34. Fukuda M, Suzuki Y, Hino H, et al. Adenosine A1 receptor blockage mediates theophylline-associated seizures. Epilepsia. 2010;51:483-487.
35. Gholipour T, Ghasemi M, Riazi K, et al. Seizure susceptibility alteration through 5-HT(3) receptor: modulation by nitric oxide. Seizure. 2010;19:17-22.
36. Gibbs E, Gibbs F. Diagnostic and localizing value of electroencephalographic studies during sleep. Res Publ Assoc Res Nerv Ment Dis. 1947;26:366-376 (abstract).
37. Gooley JJ, Rajaratnam SM, Brainard GC, et al. Spectral responses of the human circadian system depend on the irradiance and duration of exposure to light. Sci Transl Med. 2010;2:31-33.
38. Gooley JJ, Lu J, Fischer D, Saper CB. A broad role for melanopsin in nonvisual photoreception. J Neurosci. 2003;23:7093-7106. (Pubitemid 36975874)
39. Gronfier C, Wright KP Jr, Kronauer RE, Czeisler CA. Entrainment of the human circadian pacemaker to longer-than-24-h days. Proc Natl Acad Sci USA. 2007;104:9081-9086. (Pubitemid 47175440)
40. Guilhoto LM, Loddenkemper T, Vendrame M, et al. Higher evening antiepileptic drug dose for nocturnal and early-morning seizures. Epilepsy Behav. 2011; 20:334-337.
41. Gupta M, Aneja S, Kohli K. Add-on melatonin improves quality of life in epileptic children on valproate monotherapy: a randomized, double-blind, placebo-controlled trial. Epilepsy Behav. 2004;5:316-321. (Pubitemid 38950090)
42. Hasenstaub A, Sachdev RN, McCormick DA. State changes rapidly modulate cortical neuronal responsiveness. J Neurosci. 2007;27:9607-9622. (Pubitemid 47492182)
43. Herman ST, Walczak TS, Bazil CW. Distribution of partial seizures during the sleep-wake cycle: differences by seizure onset site. Neurology. 2001;56: 1453-1459. (Pubitemid 32532256)
44. Hermida RC, Ayala DE, Fernández JR, et al. Circadian rhythms in blood pressure regulation and optimization of hypertension treatment with ACE inhibitor and ARB medications. Am J Hypertens. Epub ahead of print: 7 October 2010; doi: 10.1038/ajh.2010.217.
45. Hofstra WA, de Weerd AW. How to assess circadian rhythm in humans: a review of literature. Epilepsy Behav. 2008;13:438-444.
46. Hofstra WA, de Weerd AW. The circadian rhythm and its interaction with human epilepsy: a review of literature. Sleep Med Rev. 2009;13:413-420.
47. Hofstra WA, Gordijn MC, van Hemert-van der Poel JC, et al. Chronotypes and subjective sleep parameters in epilepsy patients: a large questionnaire study. Chronobiol Int. 2010;27:1271-1286.
48. Hofstra WA, Grootemarsink BE, Dieker R, et al. Temporal distribution of clinical seizures over the 24-h day: a retrospective observational study in a tertiary epilepsy clinic. Epilepsia. 2009a;50:2019-2026.
49. Hofstra WA, Spetgens WP, Leijten FS, et al. Diurnal rhythms in seizures detected by intracranial electrocorticographic monitoring: an observational study. Epilepsy Behav. 2009b;14:617-621.
50. Janz D. The grand mal epilepsies and the sleeping-waking cycle. Epilepsia. 1962;3:69-109.
51. Jones BE. Glia, adenosine, and sleep. Neuron. 2009;61:156-157.
52. Karafin M, St Louis EK, Zimmerman MB, et al. Bimodal ultradian seizure periodicity in human mesial temporal lobe epilepsy. Seizure. 2010;19:347-351.
53. Kotagal P, Yardi N. The relationship between sleep and epilepsy. Semin Pediatr Neurol. 2008;15:42-49. (Pubitemid 351794549)
54. Laakso ML, Leinonen L, Hatonen T, et al. Melatonin, cortisol and body temperature rhythms in Lennox-Gastaut patients with or without circadian rhythm sleep disorders. J Neurol. 1993;240:410-416. (Pubitemid 23277407)
55. Landolt HP. Sleep homeostasis: a role for adenosine in humans? Biochem Pharmacol. 2008;75:2070-2079.
56. Loddenkemper T, Kotagal P. Lateralizing signs during seizures in focal epilepsy. Epilepsy Behav. 2005;7:1-17. (Pubitemid 40975275)
57. Loddenkemper T, Syed T, Burgess R. Generalized interictal epileptiform discharges are more frequent in the morning and after sleep deprivation. Epilepsia. 2007;48(suppl 6):205-206 (abstract).
58. Loddenkemper T, Vendrame M, Zarowski M, et al. Circadian patterns of pediatric seizures. Neurology. 2011;76:145-153.
59. Lowrey PL, Takahashi JS. Mammalian circadian biology: elucidating genome-wide levels of temporal organization. Annu Rev Genomics Hum Genet. 2004;5:407-441. (Pubitemid 39362752)
60. Malow BA, Lin X, Kushwaha R, Aldrich MS. Interictal spiking increases with sleep depth in temporal lobe epilepsy. Epilepsia. 1998;39:1309-1316. (Pubitemid 29005630)
61. Matos G, Andersen ML, do Valle AC, Tufik S. The relationship between sleep and epilepsy: evidence from clinical trials and animal models. J Neurol Sci. 2010;295:1-7.
62. Mattson RH, Pratt KL, Calverley JR. Electroencephalograms of epileptics following sleep deprivation. Arch Neurol. 1965;13:310-315.
63. Monti JM. The role of dorsal raphe nucleus serotonergic and non-serotonergic neurons, and of their receptors, in regulating waking and rapid eye movement (REM) sleep. Sleep Med Rev. 2010;14:319-327.
64. Niedermeyer E, Rocca U. The diagnostic significance of sleep electroencephalograms in temporal lobe epilepsy. A comparison of scalp and depth tracings. Eur Neurol. 1972;7:119-129.
65. Nobili L, Cardinale F, Magliola U, et al. Taylor's focal cortical dysplasia increases the risk of sleep-related epilepsy. Epilepsia. 2009;50:2599-2604.
66. Ohdo S. Chronotherapeutic strategy: rhythm monitoring, manipulation and disruption. Adv Drug Deliv Rev. 2010;62:859-875.
67. Ohdo S, Koyanagi S, Matsunaga N. Chronopharmacological strategies: intra- and inter-individual variability of molecular clock. Adv Drug Deliv Rev. 2010; 62:885-897.
68. Ohdo S, Nakano S, Ogawa N. Chronotoxicity of sodium valproate and its mechanisms in mice: dose-concentration-response relationship. Chronobiol Int. 1989;6:229-235. (Pubitemid 19252283)
69. Ohdo S, Nakano S, Ogawa N. Chronopharmacokinetics of valproic acid following constant-rate administration in mice. Chronobiol Int. 1991;8:35-43.
70. Ohdo S, Watanabe H, Ogawa N, et al. Circadian rhythm of embryotoxicity induced by sodium valproate in mice. Eur J Pharmacol. 1995;293:281-285.
71. Panda S, Provencio I, Tu DC, et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science. 2003;301:525-527. (Pubitemid 36900311)
72. Panda S, Sato TK, Castrucci AM, et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002;298:2213-2216. (Pubitemid 35471251)
73. Patry G, Lyagoubi S, Tassinari CA. Subclinical "electrical status epilepticus" induced by sleep in children. A clinical and electroencephalographic study of six cases. Arch Neurol. 1971;24:242-252.
74. Pavlova MK, Shea SA, Bromfield EB. Day/night patterns of focal seizures. Epilepsy Behav. 2004;5:44-49. (Pubitemid 38937063)
75. Peled N, Shorer Z, Peled E, Pillar G. Melatonin effect on seizures in children with severe neurologic deficit disorders. Epilepsia. 2001;42:1208-1210. (Pubitemid 32947944)
76. Poh M, Loddenkemper T, Swenson N, et al. Continuous monitoring of electrodermal activity during epileptic seizures using a wearable sensor. ConfProc IEEE Eng Med Biol Soc. 2010;1:4415-4418.
77. Pratt KL, Mattson RH, Weikers NJ, Williams R. EEG activation of epileptics following sleep deprivation: a prospective study of 114 cases. Electroencephalogr Clin Neurophysiol. 1968;24:11-15.
78. Pratt KL, Weikers NJ, Mattson RH, Williams RW. EEG activation after sleep deprivation. Electroencephalogr Clin Neurophysiol. 1967;23:86-87.
79. Provencio I, Jiang G, De Grip WJ, et al. Melanopsin: an opsin in melanophores, brain, and eye. Proc Natl Acad Sci USA. 1998;95:340-345. (Pubitemid 28103955)
80. Provini F, Plazzi G, Tinuper P, et al. Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases. Brain. 1999;122(Pt 6):1017-1031. (Pubitemid 29533119)
81. Pung T, Schmitz B. Circadian rhythm and personality profile in juvenile myoclonic epilepsy. Epilepsia. 2006;47(suppl 2):111-114. (Pubitemid 44684639)
82. Quigg M. Circadian rhythms: interactions with seizures and epilepsy. Epilepsy Res. 2000;42:43-55.
83. Quigg M, Straume M. Dual epileptic foci in a single patient express distinct temporal patterns dependent on limbic versus nonlimbic brain location. Ann Neurol. 2000;48:117-120. (Pubitemid 30432441)
84. Quigg M, Straume M, Menaker M, Bertram EH 3rd. Temporal distribution of partial seizures: comparison of an animal model with human partial epilepsy Ann Neurol. 1998;43:748-755. (Pubitemid 28280218)
85. Rao ML, Stefan H, Bauer J. Epileptic but not psychogenic seizures are accompanied by simultaneous elevation of serum pituitary hormones and cortisol levels. Neuroendocrinology. 1989;49:33-39. (Pubitemid 19048651)
86. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature. 2002;418:935-941. (Pubitemid 34976023)
87. Sandyk R, Tsagas N, Anninos PA. Melatonin as a proconvulsive hormone in humans. Int JNeurosci. 1992;63:125-135.
88. Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005;437:1257-1263. (Pubitemid 41568665)
89. Silverman D, Morisaki A. Re-evaluation of sleep electroencephalography. Electroencephalogr Clin Neurophysiol. 1958;10:425-431.
90. Sinha S, Brady M, Scott CA, Walker MC. Do seizures in patients with refractory epilepsy vary between wakefulness and sleep? J Neurol Neurosurg Psychiatry. 2006;77:1076-1078. (Pubitemid 44338535)
91. Song JG, Ohdo S, Ogawa N. Chronopharmacokinetics of valproic acid following constant-rate administration in mice and influence of feeding schedule. Zhongguo Yao Li Xue Bao. 1995;16:113-117.
92. Steriade M, Nunez A, Amzica F. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci. 1993a;13:3266-3283. (Pubitemid 23241167)
93. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science. 1993b;262:679-685. (Pubitemid 23350685)
94. Stewart LS, Leung LS. Hippocampal melatonin receptors modulate seizure threshold. Epilepsia. 2005;46:473-480. (Pubitemid 40470668)
95. Touchon J, Baldy-Moulinier M, Billiard M, et al. Sleep organization and epilepsy Epilepsy Res Suppl. 1991;2:73-81.
96. White P, Dyken M, Grant P, Jackson L. Electroencephalographic abnormalities during sleep as related to the temporal distribution of seizures. Epilepsia. 1962;3:167-174.
97. Wilson JV, Reynolds EH. Texts and documents. Translation and analysis of a cuneiform text forming part of a Babylonian treatise on epilepsy. Med Hist 1990;34:185-198.
98. Yegnanarayan R, Mahesh SD, Sangle S. Chronotherapeutic dose schedule of phenytoin and carbamazepine in epileptic patients. Chronobiol Int. 2006;23: 1035-1046. (Pubitemid 44595011)
99. Zaidi FH, Hull JT, Peirson SN, et al. Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Curr Biol. 2007;17:2122-2128. (Pubitemid 50014862)
100. Zarowski M, Loddenkemper T, Vendrame M, et al. Relationship of day/night and sleep/wake patterns to seizure semiology and epilepsy localization. Neurology. 2010;74(suppl 2):A105 (abstract).