Circadian rhythm and epilepsy

Advances in diagnostic technology, including chronic intracranial EEG recordings, have confirmed the clinical observation of different temporal patterns of epileptic activity and seizure occurrence over a 24-h period. The rhythmic patterns in epileptic activity and seizure occurrence are probably related to vigilance states and circadian variation in excitatory and inhibitory balance. Core circadian genes BMAL1 and CLOCK, which code for transcription factors, have been shown to influence excitability and seizure threshold. Despite uncertainties about the relative contribution of vigilance states versus circadian rhythmicity, including circadian factors such as seizure timing improves sensitivity of seizure prediction algorithms in individual patients. Improved prediction of seizure occurrence opens the possibility for personalised antiepileptic drug-dosing regimens timed to particular phases of the circadian cycle to improve seizure control and to reduce side-effects and risks associated with seizures. Further studies are needed to clarify the pathways through which rhythmic patterns of epileptic activity are generated, because this might also inform future treatment options.

[1]  Francesco Brigo,et al.  Melatonin as add-on treatment for epilepsy. , 2016, The Cochrane database of systematic reviews.

[2]  I. Scheffer,et al.  Definition and diagnostic criteria of sleep-related hypermotor epilepsy. , 2016, Neurology.

[3]  W. Gowers Epilepsy and Other Chronic Convulsive Diseases: Their Causes, Symptoms, and Treatment , 2008 .

[4]  Moritz Heinrich Romberg,et al.  A Manual of the Nervous Diseases of Man , 1844, The British and foreign medical review.

[5]  C. A. Marsan,et al.  Cellular Mechanisms in Experimental Epileptic Seizures , 1964, Science.

[6]  D. Janz Die Epilepsien : spezielle Pathologie und Therapie , 1969 .

[7]  T. Hirfanoğlu,et al.  Sleep-wake distribution and circadian patterns of epileptic seizures in children. , 2016, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[8]  Morningness and eveningness: When do patients take their antiepileptic drugs? , 2012, Epilepsy & Behavior.

[9]  S. Daan,et al.  The two‐process model of sleep regulation: a reappraisal , 2016, Journal of sleep research.

[10]  G. Worrell,et al.  Seizure Forecasting from Idea to Reality. Outcomes of the My Seizure Gauge Epilepsy Innovation Institute Workshop , 2017, eNeuro.

[11]  Levin Kuhlmann,et al.  The circadian profile of epilepsy improves seizure forecasting , 2017, Brain : a journal of neurology.

[12]  S. Shorvon,et al.  Longitudinal cohort studies of the prognosis of epilepsy: contribution of the National General Practice Study of Epilepsy and other studies. , 2013, Brain : a journal of neurology.

[13]  David M. Himes,et al.  Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study , 2013, The Lancet Neurology.

[14]  S. Sangle,et al.  Chronotherapeutic Dose Schedule of Phenytoin and Carbamazepine in Epileptic Patients , 2006, Chronobiology international.

[15]  T. Loddenkemper,et al.  Circadian patterns of pediatric seizures , 2011, Neurology.

[16]  B. Bruguerolle,et al.  Chronopharmacokinetics , 1998, Clinical pharmacokinetics.

[17]  R. Manni,et al.  Circadian phase typing in idiopathic generalized epilepsy: Dim light melatonin onset and patterns of melatonin secretion—Semicurve findings in adult patients , 2016, Epilepsy & Behavior.

[18]  L. Tassi,et al.  Sleep-related epileptic behaviors and non-REM-related parasomnias: Insights from stereo-EEG. , 2016, Sleep medicine reviews.

[19]  M. Steriade Sleep, epilepsy and thalamic reticular inhibitory neurons , 2005, Trends in Neurosciences.

[20]  Catharine L. Smith,et al.  Valproic acid disrupts the oscillatory expression of core circadian rhythm transcription factors , 2018, Toxicology and applied pharmacology.

[21]  C. Schmidt,et al.  Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations , 2017, Scientific Reports.

[22]  T. Loddenkemper,et al.  Sleep-wake patterns of seizures in children with lesional epilepsy. , 2011, Pediatric neurology.

[23]  S. Schuele,et al.  Chronotypes in Patients with Epilepsy: Does the Type of Epilepsy Make a Difference? , 2015, Behavioural neurology.

[24]  David M. Sabatini,et al.  mTOR Signaling in Growth, Metabolism, and Disease , 2017, Cell.

[25]  Derk-Jan Dijk,et al.  Circadian regulation of slow waves in human sleep: Topographical aspects , 2015, NeuroImage.

[26]  L. Castro,et al.  Gender and age influence in daytime and nighttime seizure occurrence in epilepsy associated with mesial temporal sclerosis , 2015, Epilepsy & Behavior.

[27]  T. Güttler,et al.  The Circadian Protein BMAL1 Regulates Translation in Response to S6K1-Mediated Phosphorylation , 2015, Cell.

[28]  S. Baxendale,et al.  Bright light therapy as an add on treatment for medically intractable epilepsy , 2012, Epilepsy & Behavior.

[29]  A. Szűcs,et al.  The role of NREM sleep micro-arousals in absence epilepsy and in nocturnal frontal lobe epilepsy , 2013, Epilepsy Research.

[30]  K. Fent,et al.  Effects of diazepam on gene expression and link to physiological effects in different life stages in zebrafish Danio rerio. , 2010, Environmental science & technology.

[31]  M. Newton,et al.  Sleep deprivation increases cortical excitability in epilepsy , 2006, Neurology.

[32]  J. Hogenesch,et al.  mTOR signaling regulates central and peripheral circadian clock function , 2018, PLoS genetics.

[33]  Tobias Loddenkemper,et al.  Patterns of epileptic seizure occurrence , 2019, Brain Research.

[34]  M. Curtis,et al.  Circadian clustering of spontaneous epileptic seizures emerges after pilocarpine‐induced status epilepticus , 2017, Epilepsia.

[35]  G. Charpentier,et al.  Customization of home closed-loop insulin delivery in adult patients with type 1 diabetes, assisted with structured remote monitoring: the pilot WP7 Diabeloop study , 2018, Acta Diabetologica.

[36]  Marcello Massimini,et al.  Circadian regulation of human cortical excitability , 2016, Nature Communications.

[37]  M Steriade,et al.  Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. , 2000, Journal of neurophysiology.

[38]  Julien Q. M. Ly,et al.  Circadian dynamics in measures of cortical excitation and inhibition balance , 2016, Scientific Reports.

[39]  D.G.M. Dijk,et al.  Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  S. Hong,et al.  Sleep–wake pattern, chronotype and seizures in patients with epilepsy , 2016, Epilepsy Research.

[41]  R. E. Madsen,et al.  EEG Signal Quality of a Subcutaneous Recording System Compared to Standard Surface Electrodes , 2015, J. Sensors.

[42]  C. Colwell,et al.  Circadian regulation of a-type potassium currents in the suprachiasmatic nucleus. , 2010, Journal of neurophysiology.

[43]  Martin Straume,et al.  Temporal distribution of partial seizures: Comparison of an animal model with human partial epilepsy , 1998, Annals of neurology.

[44]  J. Gerstner,et al.  BMAL1 controls the diurnal rhythm and set point for electrical seizure threshold in mice , 2014, Front. Syst. Neurosci..

[45]  M. Gordijn,et al.  CHRONOTYPES AND SUBJECTIVE SLEEP PARAMETERS IN EPILEPSY PATIENTS: A LARGE QUESTIONNAIRE STUDY , 2010, Chronobiology international.

[46]  M. Straume,et al.  Dual epileptic foci in a single patient express distinct temporal patterns dependent on limbic versus nonlimbic brain location , 2000, Annals of neurology.

[47]  T. Paiva,et al.  24-hour rhythmicity of seizures in refractory focal epilepsy , 2016, Epilepsy & Behavior.

[48]  T. Loddenkemper,et al.  Chronopharmacology of Anti-Convulsive Therapy , 2013, Current Neurology and Neuroscience Reports.

[49]  B. Högl,et al.  Sleep disorders and circadian rhythm in epilepsy revisited: a prospective controlled study. , 2015, Sleep medicine.

[50]  G. Vandewalle,et al.  Local modulation of human brain responses by circadian rhythmicity and sleep debt , 2016, Science.

[51]  F. Scheer,et al.  Is there a circadian variation of epileptiform abnormalities in idiopathic generalized epilepsy? , 2009, Epilepsy & Behavior.

[52]  I. Scheffer,et al.  Mutations in mammalian target of rapamycin regulator DEPDC5 cause focal epilepsy with brain malformations , 2014, Annals of neurology.

[53]  K. Staley Molecular mechanisms of epilepsy , 2015, Nature Neuroscience.

[54]  R. Manni,et al.  Chronotype in patients with epilepsy: A controlled study in 60 subjects with late-onset focal epilepsy , 2015, Epilepsy & Behavior.

[55]  I. Scheffer,et al.  Mutations in the mammalian target of rapamycin pathway regulators NPRL2 and NPRL3 cause focal epilepsy , 2015, Annals of neurology.

[56]  C. Saper,et al.  Hypothalamic regulation of sleep and circadian rhythms , 2005, Nature.

[57]  A. Reinberg,et al.  Chronotolerance study of the antiepileptic drug valproic acid in mice , 2012, Journal of circadian rhythms.

[58]  Kenji F. Tanaka,et al.  Near-infrared deep brain stimulation via upconversion nanoparticle–mediated optogenetics , 2018, Science.

[59]  G. Ko,et al.  Circadian regulation of ion channels and their functions , 2009, Journal of neurochemistry.

[60]  Paul D. Gamlin,et al.  Measuring and using light in the melanopsin age , 2014, Trends in Neurosciences.

[61]  Ueli Schibler,et al.  The loss of circadian PAR bZip transcription factors results in epilepsy. , 2004, Genes & development.

[62]  B. Bourgeois,et al.  Higher evening antiepileptic drug dose for nocturnal and early-morning seizures , 2011, Epilepsy & Behavior.

[63]  H. Goodkin,et al.  Loss of CLOCK Results in Dysfunction of Brain Circuits Underlying Focal Epilepsy , 2017, Neuron.

[64]  J. French,et al.  Adjunctive everolimus therapy for treatment-resistant focal-onset seizures associated with tuberous sclerosis (EXIST-3): a phase 3, randomised, double-blind, placebo-controlled study , 2016, The Lancet.

[65]  T. Loddenkemper,et al.  Circadian distribution and sleep/wake patterns of generalized seizures in children , 2011, Epilepsia.

[66]  I. Soltesz,et al.  Future of seizure prediction and intervention: closing the loop. , 2015, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[67]  T. Loddenkemper,et al.  Long-term response to high-dose diazepam treatment in continuous spikes and waves during sleep. , 2013, Pediatric neurology.

[68]  Emily A. Mirro,et al.  Multi-day rhythms modulate seizure risk in epilepsy , 2018, Nature Communications.

[69]  Tobias Loddenkemper,et al.  Clobazam higher-evening differential dosing as an add-on therapy in refractory epilepsy , 2016, Seizure.

[70]  K. Gamble,et al.  Circadian clock control of endocrine factors , 2014, Nature Reviews Endocrinology.

[71]  Ying-Hui Fu,et al.  Human genetics and sleep behavior , 2017, Current Opinion in Neurobiology.

[72]  S. Danzer,et al.  Mechanisms regulating neuronal excitability and seizure development following mTOR pathway hyperactivation , 2014, Front. Mol. Neurosci..

[73]  Boyoung Lee,et al.  Mammalian Target of Rapamycin Signaling Modulates Photic Entrainment of the Suprachiasmatic Circadian Clock , 2010, The Journal of Neuroscience.

[74]  J. Takahashi,et al.  Molecular architecture of the mammalian circadian clock. , 2014, Trends in cell biology.

[75]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[76]  C. Randler,et al.  Circadian Typology: A Comprehensive Review , 2012, Chronobiology international.

[77]  N. Sonenberg,et al.  mTOR signaling in VIP neurons regulates circadian clock synchrony and olfaction , 2018, Proceedings of the National Academy of Sciences.

[78]  T. Loddenkemper,et al.  Predicting diurnal and sleep/wake seizure patterns in paediatric patients of different ages. , 2014, Epileptic disorders : international epilepsy journal with videotape.

[79]  A. Wirz-Justice,et al.  Life between Clocks: Daily Temporal Patterns of Human Chronotypes , 2003, Journal of biological rhythms.

[80]  M. Joëls,et al.  Seizure occurrence and the circadian rhythm of cortisol: a systematic review , 2015, Epilepsy & Behavior.

[81]  D. Plenz,et al.  Intrinsic excitability measures track antiepileptic drug action and uncover increasing/decreasing excitability over the wake/sleep cycle , 2015, Proceedings of the National Academy of Sciences.

[82]  Johannes Van Dijk,et al.  Multimodal, automated detection of nocturnal motor seizures at home: Is a reliable seizure detector feasible? , 2017, Epilepsia open.

[83]  Mark Quigg,et al.  Circadian and ultradian patterns of epileptiform discharges differ by seizure‐onset location during long‐term ambulatory intracranial monitoring , 2016, Epilepsia.

[84]  Felice T. Sun,et al.  Day–Night Patterns of Epileptiform Activity in 65 Patients With Long-Term Ambulatory Electrocorticography , 2015, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[85]  Christos G. Gkogkas,et al.  Translational Control of Entrainment and Synchrony of the Suprachiasmatic Circadian Clock by mTOR/4E-BP1 Signaling , 2013, Neuron.