Temporal distributions of seizure occurrence from various epileptogenic regions

Objective: The aim of this study was to determine whether seizure occurrence in partial epilepsy is under the influence of circadian rhythms and rhythmic exogenous factors, and how this influence varies according to cortical brain region. For these ends, we determined and analyzed detailed temporal distributions of seizures arising from the frontal, parietal, occipital, neocortical temporal, and mesial temporal lobes. Methods: We retrospectively analyzed intracranial EEG recordings from 131 consecutive adult subjects whose partial epilepsy was sufficiently localized for surgical resection. In all, 669 seizures were analyzed: 132 frontal, 77 parietal, 83 occipital, 217 mesial temporal, and 160 neocortical temporal. Results: Seizure distribution was dependent on brain region (p < 10−9). Nonuniform seizure distributions were observed in the parietal (p < 10−4), occipital (p < 10−7), mesial temporal (p < 0.02), and neocortical temporal lobes (p < 0.04). Occipital and parietal seizures occurred in strong gaussian-like distributions, 180° out of phase relative to each other; occipital seizure occurrence peaked between 16:00 and 19:00, whereas parietal seizures peaked between 4:00 and 7:00. Frontal lobe seizures followed a unimodal distribution, peaking between 4:00 and 7:00. Seizures from the mesial temporal lobe were distributed bimodally, with the primary peak in the late afternoon between 16:00 and 19:00 and secondary peak in the morning between 7:00 and 10:00. Neocortical temporal seizures peaked slightly before the primary peak observed in the mesial temporal lobe; however, these distributions did not differ significantly. Conclusions: Seizure occurrence in partial epilepsy is not random. Endogenous circadian rhythms and rhythmic exogenous factors likely play substantial roles in seizure occurrence. These roles vary considerably according to brain region. Frontal and parietal lobe seizures seem most likely to occur nocturnally, whereas occipital and temporal lobe seizures seem to have strong afternoon preferences.

[1]  T. Salmi,et al.  Circadian rhythm studies in neuronal ceroid-lipofuscinosis (NCL). , 1995, American journal of medical genetics.

[2]  T. Baram,et al.  High-dose corticotropin (ACTH) versus prednisone for infantile spasms: a prospective, randomized, blinded study. , 1996, Pediatrics.

[3]  S. Shorvon,et al.  Plasma concentrations of prolactin, noradrenaline, vasopressin and oxytocin during and after a prolonged epileptic seizure , 1994, Acta neurologica Scandinavica.

[4]  B Diehl,et al.  Temporal Lobe Epilepsy: When Are Invasive Recordings Needed? , 2000, Epilepsia.

[5]  M. Modugno,et al.  Autosomal dominant nocturnal frontal lobe epilepsy. A video-polysomnographic and genetic appraisal of 40 patients and delineation of the epileptic syndrome. , 1998, Brain : a journal of neurology.

[6]  R. McCarley,et al.  Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. , 1997, Science.

[7]  S. Campbell,et al.  Physiology of the circadian system in animals and humans. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[8]  L. Stewart,et al.  Hippocampal Melatonin Receptors Modulate Seizure Threshold , 2005, Epilepsia.

[9]  L. Tecott,et al.  Global Increases in Seizure Susceptibility in Mice Lacking 5-HT2CReceptors: A Behavioral Analysis , 1998, Experimental Neurology.

[10]  B. Malow,et al.  Relationship of epileptic seizures to sleep stage and sleep depth. , 2002, Sleep.

[11]  S. Moshé,et al.  Seizure Lateralization During EEG Monitoring in Patients with Bilateral Foci: The Cluster Effect , 1997, Epilepsia.

[12]  R. Stephenson Do circadian rhythms in respiratory control contribute to sleep-related breathing disorders? , 2003, Sleep medicine reviews.

[13]  M. Lucock,et al.  Daily Variations in Steady-State Plasma Concentrations of Carbamazepine and its Metabolites in Epileptic Children , 1991, Clinical pharmacokinetics.

[14]  B. Pappas,et al.  Potentiation of amygdala kindling in adult or infant rats by injections of 6-hydroxydopamine , 1979, Experimental Neurology.

[15]  R. Reiter,et al.  Melatonin's Role as an Anticonvulsant and Neuronal Protector: Experimental and Clinical Evidence , 1998, Journal of child neurology.

[16]  M. Sperling,et al.  Prolactin in partial epilepsy: An indicator of limbic seizures , 1986, Annals of neurology.

[17]  L. Tuomisto,et al.  Modifying effects of histamine on circadian rhythms and neuronal excitability , 2001, Behavioural Brain Research.

[18]  J. Koolhaas,et al.  High-voltage-activated Ca2+ currents and the excitability of pyramidal neurons in the hippocampal CA3 subfield in rats depend on corticosterone and time of day , 2001, Neuroscience Letters.

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

[20]  E. Ingelsson,et al.  Diurnal blood pressure pattern and risk of congestive heart failure. , 2006, JAMA.

[21]  C. Matthews,et al.  Melatonin Response in Active Epilepsy , 1995, Epilepsia.

[22]  G. Rosadini,et al.  Sleep-EEG modulation of interictal epileptiform discharges in adult partial epilepsy: a spectral analysis study , 2000, Clinical Neurophysiology.

[23]  B. dalla Bernardina,et al.  Sleep and benign partial epilepsies of childhood: EEG and evoked potentials study. , 1991, Epilepsy research. Supplement.

[24]  A. Desautels,et al.  Circadian variation of the effects of immobility on symptoms of restless legs syndrome. , 2005, Sleep.

[25]  R. McCarley,et al.  Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study , 2000, Neuroscience.

[26]  David A. Freedman,et al.  On the maximum deviation between the histogram and the underlying density , 1981 .

[27]  C A Czeisler,et al.  Variation of electroencephalographic activity during non‐rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans , 1997, The Journal of physiology.

[28]  G. Solomon,et al.  Circadian rhythms and migraine. , 1992, Cleveland Clinic journal of medicine.

[29]  J. Gotman,et al.  A study of the transition from spindles to spike and wave discharge in feline generalized penicillin epilepsy: Microphysiological features , 1981, Experimental Neurology.

[30]  Sheryl R. Haut Seizure clustering , 2006, Epilepsy & Behavior.

[31]  W. Russell Brain,et al.  TIME OF DAY IN RELATION TO CONVULSIONS IN EPILEPSY. , 1929 .

[32]  E. Haus,et al.  Circadian Variation in Stroke Onset: Identical Temporal Pattern in Ischemic and Hemorrhagic Events , 2005, Chronobiology international.

[33]  M. Sammaritano,et al.  Effect of anticonvulsants on sleep. , 2000, Neurology.

[34]  K. Eagle,et al.  Chronobiology of rupture and dissection of aortic aneurysms. , 2004, Journal of vascular surgery.

[35]  D. Boison Adenosine and Epilepsy: From Therapeutic Rationale to New Therapeutic Strategies , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  S. Gunatilake The Course of epilepsy , 1996 .

[37]  E. Speckmann,et al.  Melatonin receptors in rat hippocampus: molecular and functional investigations , 2002, Hippocampus.

[38]  S. Shea,et al.  Day/night patterns of focal seizures , 2004, Epilepsy & Behavior.

[39]  M. Sammaritano,et al.  Distribution of partial seizures during the sleep–wake cycle , 2001, Neurology.

[40]  J. Tylor Fox,et al.  RHYTHM IN EPILEPSY , 1938 .

[41]  W R Jankel,et al.  Sleep Spindles , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[42]  T S Walczak,et al.  Effects of Sleep and Sleep Stage on Epileptic and Nonepileptic Seizures , 1997, Epilepsia.

[43]  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.

[44]  P. Coubes,et al.  The Relationship Between Sleep and Epilepsy in Frontal and Temporal Lobe Epilepsies: Practical and Physiopathologic Considerations , 1998, Epilepsia.

[45]  J. Burchfiel,et al.  Kindling antagonism: Effects of norepinephrine depletion on kindled seizure suppression after concurrent, alternate stimulation in rats , 1986, Experimental Neurology.

[46]  M. Straume,et al.  Hypothalamic Neuronal Loss and Altered Circadian Rhythm of Temperature in a Rat Model of Mesial Temporal Lobe Epilepsy , 1999, Epilepsia.

[47]  M. Aldrich,et al.  Interictal Spiking Increases with Sleep Depth in Temporal Lobe Epilepsy , 1998, Epilepsia.