Effect of Seizures on the Developing Brain and Cognition

Committee on the Public Health Dimensions of the Epilepsies, Board on Health Sciences Policy, and Institute of Medicine: Epilepsy Across the Spectrum: Promoting Health and Understanding. The National Academies Press, 2012 Holmes, 2015, Cognitive impairment in epilepsy: The role of network abnormalities, Epileptic Disord, 17, 101, 10.1684/epd.2015.0739 Holmes, 2014, What is more harmful, seizures or epileptic EEG abnormalities? Is there any clinical data?, Epileptic Disord, 16, S12 Farwell, 1985, Neuropsychological abilities of children with epilepsy, Epilepsia, 26, 395, 10.1111/j.1528-1157.1985.tb05670.x Neyens, 1999, Prospective follow-up of intellectual development in children with a recent onset of epilepsy, Epilepsy Res, 34, 85, 10.1016/S0920-1211(98)00118-1 Sillanpaa, 1998, Long-term prognosis of seizures with onset in childhood, N Engl J Med, 338, 1715, 10.1056/NEJM199806113382402 Prasad, 2014, Epilepsy, comorbid conditions in Canadian children: Analysis of cross-sectional data from cycle 3 of the National Longitudinal Study of Children and Youth, Seizure, 23, 869, 10.1016/j.seizure.2014.07.012 Buelow, 2012, Adaptive functioning in children with epilepsy and learning problems, J Child Neurol, 27, 1241, 10.1177/0883073811432750 Bailet, 2000, The impact of childhood epilepsy on neurocognitive and behavioral performance: A prospective longitudinal study, Epilepsia, 41, 426, 10.1111/j.1528-1157.2000.tb00184.x Wakamoto, 2000, Long-term medical, educational, and social prognoses of childhood-onset epilepsy: A population-based study in a rural district of Japan, Brain Dev, 22, 246, 10.1016/S0387-7604(00)00121-2 Williams, 1998, Neuropsychological patterns in pediatric epilepsy, Seizure, 7, 223, 10.1016/S1059-1311(98)80040-X Bourgeois, 1983, Intelligence in epilepsy: A prospective study in children, Ann Neurol, 14, 438, 10.1002/ana.410140407 Hermann, 2002, The neurodevelopmental impact of childhood onset temporal lobe epilepsy on brain structure and function and the risk of progressive cognitive effects, Prog Brain Res, 135, 429, 10.1016/S0079-6123(02)35040-4 Berg, 2012, Age at onset of epilepsy, pharmacoresistance, and cognitive outcomes: A prospective cohort study, Neurology, 79, 1384, 10.1212/WNL.0b013e31826c1b55 Nabbout, 2003, Epileptic encephalopathies: A brief overview, J Clin Neurophysiol, 20, 393, 10.1097/00004691-200311000-00002 Shields, 2000, Catastrophic epilepsy in childhood, Epilepsia, 41, S2, 10.1111/j.1528-1157.2000.tb01518.x Berg, 2010, Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005-2009, Epilepsia, 51, 676, 10.1111/j.1528-1167.2010.02522.x Glass, 2009, Clinical neonatal seizures are independently associated with outcome in infants at risk for hypoxic-ischemic brain injury, J Pediatr, 155, 318, 10.1016/j.jpeds.2009.03.040 Korman, 2013, Early seizure onset and dysplastic lesion extent independently disrupt cognitive networks, Neurology, 81, 745, 10.1212/WNL.0b013e3182a1aa2a Kalume, 2007, Reduced sodium current in Purkinje neurons from Nav1.1 mutant mice: Implications for ataxia in severe myoclonic epilepsy in infancy, J Neurosci, 27, 11065, 10.1523/JNEUROSCI.2162-07.2007 Oakley, 2009, Temperature- and age-dependent seizures in a mouse model of severe myoclonic epilepsy in infancy, Proc Natl Acad Sci U S A, 106, 3994, 10.1073/pnas.0813330106 Ogiwara, 2007, Na(v)1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: A circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation, J Neurosci, 27, 5903, 10.1523/JNEUROSCI.5270-06.2007 Chen, 2004, Mice lacking sodium channel beta1 subunits display defects in neuronal excitability, sodium channel expression, and nodal architecture, J Neurosci, 24, 4030, 10.1523/JNEUROSCI.4139-03.2004 Tang, 2009, A BAC transgenic mouse model reveals neuron subtype-specific effects of a Generalized Epilepsy with Febrile Seizures Plus (GEFS+) mutation, Neurobiol Dis, 35, 91, 10.1016/j.nbd.2009.04.007 Martin, 2010, Altered function of the SCN1A voltage-gated sodium channel leads to gamma-aminobutyric acid-ergic (GABAergic) interneuron abnormalities, J Biol Chem, 285, 9823, 10.1074/jbc.M109.078568 Sun, 2012, A knock-in model of human epilepsy in Drosophila reveals a novel cellular mechanism associated with heat-induced seizure, J Neurosci, 32, 14145, 10.1523/JNEUROSCI.2932-12.2012 Schutte, 2014, Knock-in model of Dravet syndrome reveals a constitutive and conditional reduction in sodium current, J Neurophysiol, 112, 903, 10.1152/jn.00135.2014 Wagnon, 2015, Convulsive seizures and SUDEP in a mouse model of SCN8A epileptic encephalopathy, Hum Mol Genet, 24, 506, 10.1093/hmg/ddu470 Han, 2012, Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission, Nature, 489, 385, 10.1038/nature11356 Ito, 2013, Mouse with Nav1.1 haploinsufficiency, a model for Dravet syndrome, exhibits lowered sociability and learning impairment, Neurobiol Dis, 49, 29, 10.1016/j.nbd.2012.08.003 Ohmori, 2014, Methylphenidate improves learning impairments and hyperthermia-induced seizures caused by an Scn1a mutation, Epilepsia, 55, 1558, 10.1111/epi.12750 Sawyer, 2016, Scn1a dysfunction alters behavior but not the effect of stress on seizure response, Genes Brain Behav, 15, 335, 10.1111/gbb.12281 Bender, 2013, Focal Scn1a knockdown induces cognitive impairment without seizures, Neurobiol Dis, 54, 297, 10.1016/j.nbd.2012.12.021 Barry, 2015, T2 relaxation time post febrile status epilepticus predicts cognitive outcome, Exp Neurol, 269, 242, 10.1016/j.expneurol.2015.04.015 Choy, 2014, A novel, noninvasive, predictive epilepsy biomarker with clinical potential, J Neurosci, 34, 8672, 10.1523/JNEUROSCI.4806-13.2014 Dube, 2008, Cognitive dysfunction after experimental febrile seizures, Exp Neurol, 215, 167, 10.1016/j.expneurol.2008.10.003 Dube, 2006, Temporal lobe epilepsy after experimental prolonged febrile seizures: Prospective analysis, Brain, 129, 911, 10.1093/brain/awl018 Dubé, 2006, Complex febrile seizures—An experimental model in immature rodents, 333 Karnam, 2009, Effect of age on cognitive sequelae following early life seizures in rats, Epilepsy Res, 85, 221, 10.1016/j.eplepsyres.2009.03.008 Kleen, 2011, Enhanced oscillatory activity in the hippocampal-prefrontal network is related to short-term memory function after early-life seizures, J Neurosci, 31, 15397, 10.1523/JNEUROSCI.2196-11.2011 Lucas, 2011, Impaired cognition in rats with cortical dysplasia: Additional impact of early-life seizures, Brain, 134, 1684, 10.1093/brain/awr087 Kleen, 2011, Early-life seizures produce lasting alterations in the structure and function of the prefrontal cortex, Epilepsy Behav, 22, 214, 10.1016/j.yebeh.2011.07.022 Karnam, 2009, Early life seizures cause long-standing impairment of the hippocampal map, Exp Neurol, 217, 378, 10.1016/j.expneurol.2009.03.028 Zhou, 2007, Impaired single cell firing and long-term potentiation parallels memory impairment following recurrent seizures, Eur J Neurosci, 25, 3667, 10.1111/j.1460-9568.2007.05598.x Hoffmann, 2004, Cognitive impairment following status epilepticus and recurrent seizures during early development: Support for the “two-hit hypothesis”, Epilepsy Behav, 5, 873, 10.1016/j.yebeh.2004.09.005 de Rogalski Landrot, 2001, Recurrent neonatal seizures: Relationship of pathology to the electroencephalogram and cognition, Brain Res Dev Brain Res, 129, 27, 10.1016/S0165-3806(01)00177-8 Huang, 1999, Long-term effects of neonatal seizures: A behavioral, electrophysiological, and histological study, Brain Res Dev Brain Res, 118, 99, 10.1016/S0165-3806(99)00135-2 Lugo, 2014, Early-life seizures result in deficits in social behavior and learning, Exp Neurol, 256, 74, 10.1016/j.expneurol.2014.03.014 Neill, 1996, Recurrent seizures in immature rats: Effect on auditory and visual discrimination, Brain Res Dev Brain Res, 95, 283, 10.1016/0165-3806(96)00099-5 Holmes, 2015, Alterations in sociability and functional brain connectivity caused by early-life seizures are prevented by bumetanide, Neurobiol Dis, 77, 204, 10.1016/j.nbd.2015.02.015 Holmes, 1999, Mossy fiber sprouting after recurrent seizures during early development in rats, J Comp Neurol, 404, 537, 10.1002/(SICI)1096-9861(19990222)404:4<537::AID-CNE9>3.0.CO;2-# Holmes, 1998, Consequences of neonatal seizures in the rat: Morphological and behavioral effects, Ann Neurol, 44, 845, 10.1002/ana.410440602 McCabe, 2001, Reduced neurogenesis after neonatal seizures, J Neurosci, 21, 2094, 10.1523/JNEUROSCI.21-06-02094.2001 Isaeva, 2006, Selective impairment of GABAergic synaptic transmission in the flurothyl model of neonatal seizures, Eur J Neurosci, 23, 1559, 10.1111/j.1460-9568.2006.04693.x Isaeva, 2009, Long-term suppression of GABAergic activity by neonatal seizures in rat somatosensory cortex, Epilepsy Res, 87, 286, 10.1016/j.eplepsyres.2009.09.011 Isaeva, 2010, Recurrent neonatal seizures result in long-term increases in neuronal network excitability in the rat neocortex, Eur J Neurosci, 31, 1446, 10.1111/j.1460-9568.2010.07179.x Villeneuve, 2000, Neonatal seizures induced persistent changes in intrinsic properties of CA1 rat hippocampal cells, Ann Neurol, 47, 729, 10.1002/1531-8249(200006)47:6<729::AID-ANA5>3.0.CO;2-C Hernan, 2013, Altered short-term plasticity in the prefrontal cortex after early life seizures, Neurobiol Dis, 50, 120, 10.1016/j.nbd.2012.10.007 Isaeva, 2013, Alteration of synaptic plasticity by neonatal seizures in rat somatosensory cortex, Epilepsy Res, 106, 280, 10.1016/j.eplepsyres.2013.03.011 O’Keefe, 1971, The hippocampus as a spatial map: Preliminary evidence from unit activity in the freely-moving rat, Brain Res, 34, 171, 10.1016/0006-8993(71)90358-1 O’Keefe, 1973, Place units in the hippocampus of freely moving rats, Exp Neurol, 51, 78, 10.1016/0014-4886(76)90055-8 Lenck-Santini, 2002, Relationships between place cell firing fields and navigational decisions by rats, J Neurosci, 22, 9035, 10.1523/JNEUROSCI.22-20-09035.2002 Lenck-Santini, 2001, Evidence for a relationship between place-cell spatial firing and spatial memory performance, Hippocampus, 11, 377, 10.1002/hipo.1052 Lenck-Santini, 2008, Altered phase precession and compression of temporal sequences by place cells in epileptic rats, J Neurosci, 28, 5053, 10.1523/JNEUROSCI.5024-07.2008 Liu, 2003, Seizure-induced changes in place cell physiology: Relationship to spatial memory, J Neurosci, 23, 11505, 10.1523/JNEUROSCI.23-37-11505.2003 O’Keefe, 1993, Phase relationships between hippocampal place units and the EEG theta rhythm, Hippocampus, 3, 317, 10.1002/hipo.450030307 Skaggs, 1993, An information-theoretic approach to deciphering the hippocampal code, vol. 5, 1030 Winson, 1978, Loss of hippocampal theta rhythm results in spatial memory deficit in the rat, Science, 201, 160, 10.1126/science.663646 Gupta, 2012, Segmentation of spatial experience by hippocampal theta sequences, Nat Neurosci, 15, 1032, 10.1038/nn.3138 Colgin, 2009, Frequency of gamma oscillations routes flow of information in the hippocampus, Nature, 462, 353, 10.1038/nature08573 Steffenach, 2002, Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells, Proc Natl Acad Sci U S A, 99, 3194, 10.1073/pnas.042700999 Kleen, 2010, Hippocampal interictal spikes disrupt cognition in rats, Ann Neurol, 67, 250, 10.1002/ana.21896 Kleen, 2013, Hippocampal interictal epileptiform activity disrupts cognition in humans, Neurology, 81, 18, 10.1212/WNL.0b013e318297ee50 Krauss, 1997, Mesial temporal spikes interfere with working memory, Neurology, 49, 975, 10.1212/WNL.49.4.975 Zhou, 2007, Effect of interictal spikes on single-cell firing patterns in the hippocampus, Epilepsia, 48, 720, 10.1111/j.1528-1167.2006.00972.x Urrestarazu, 2006, High-frequency intracerebral EEG activity (100–500Hz) following interictal spikes, Epilepsia, 47, 1465, 10.1111/j.1528-1167.2006.00618.x Baumbach, 1981, Visuocortical epileptiform discharges in rabbits: Differential effects on neuronal development in the lateral geniculate nucleus and superior colliculus, Brain Res, 209, 61, 10.1016/0006-8993(81)91172-0 Ostrach, 1984, Effects of bicuculline-induced epileptiform activity on development of receptive field properties in striate cortex and lateral geniculate nucleus of the rabbit, Brain Res, 317, 113, 10.1016/0165-3806(84)90146-9 Hernan, 2014, Focal epileptiform activity in the prefrontal cortex is associated with long-term attention and sociability deficits, Neurobiol Dis, 63, 25, 10.1016/j.nbd.2013.11.012 Khan, 2010, Interictal spikes in developing rats cause long-standing cognitive deficits, Neurobiol Dis, 39, 362, 10.1016/j.nbd.2010.05.002