Persistence of Cortical Sensory Processing during Absence Seizures in Human and an Animal Model: Evidence from EEG and Intracellular Recordings

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Chipaux, Mathilde ^a,b   Vercueil, Laurent ^c   Kaminska, Anna ^d   Mahon, Séverine ^a   Charpier, Stéphane ^a,e  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b Pediatric Neurosurgery Unit   (France)

^c GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ETIRACETAM; LAMOTRIGINE; VALPROIC ACID;

ABSENCE; ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CHILD; CLINICAL ARTICLE; CONSCIOUSNESS; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; EPILEPSY; EVENT RELATED POTENTIAL; EVOKED VISUAL RESPONSE; HUMAN; HUMAN CELL; LATENT PERIOD; NERVE CELL EXCITABILITY; NONHUMAN; OSCILLATION; PRESCHOOL CHILD; PYRAMIDAL NERVE CELL; RAT; SCHOOL CHILD; SEIZURE; SENSORY STIMULATION; SENSORY SYSTEM; SOMATOSENSORY CORTEX; SPIKE WAVE; THALAMOCORTICAL TRACT; VISUAL STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; CHILD; ELECTROENCEPHALOGRAPHY; EPILEPSY, ABSENCE; EVOKED POTENTIALS; FRANCE; HUMANS; PYRAMIDAL TRACTS; RATS; SOMATOSENSORY CORTEX; SPECIES SPECIFICITY; STATISTICS, NONPARAMETRIC; TOUCH PERCEPTION;

EID: 84874608991     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058180     Document Type: Article

References (81)

1. Panayiotopoulos CP, Koutroumanidis M, Giannakodimos S, Agathonikou A, (1997) Idiopathic generalised epilepsy in adults manifested by phantom absences, generalised tonic-clonic seizures, and frequent absence status. J Neurol Neurosurg Psychiatry 63: 622-627.
2. Blumenfeld H, (2005) Consciousness and epilepsy: why are patients with absence seizures absent? Prog Brain Res 150: 271-286.
3. Panayiotopoulos CP, (2008) Typical absence seizures and related epileptic syndromes: assessment of current state and directions for future research. Epilepsia 49: 2131-2139.
4. Cavanna AE, Monaco F, (2009) Brain mechanisms of altered conscious states during epileptic seizures. Nat Rev Neurol 5: 267-276.
5. Gibbs F, Davis H, Lennox WG, (1935) The electroencephalogram in epilepsy and in conditions of impaired consciousness. Arch Neurol Psychiatr 34: 1133-1148.
6. Williams D, (1953) A study of thalamic and cortical rhythms in petit mal. Brain 76: 50-69.
7. Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, et al. (2010) Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005-2009. Epilepsia 51: 676-685.
8. Lemieux J, Blume WT, (1986) Topographical evolution of spike-wave complexes. Brain Res 373: 275-287.
9. Blume W, Lemieux JF, (1988) Morphology of spikes in spike-and-wave complexes. Electroencephalogr Clin Neurophysiol. 69: 508-515.
10. Holmes MD, Brown M, Tucker DM, (2004) Are "generalized" seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 45: 1568-1579.
11. Sadleir LG, Farrell K, Smith S, Connolly MB, Scheffer IE, (2006) Electroclinical features of absence seizures in childhood absence epilepsy. Neurology 67: 413-418.
12. Westmijse I, Ossenblok P, Gunning B, van Luijtelaar G, (2009) Onset and propagation of spike and slow wave discharges in human absence epilepsy: A MEG study. Epilepsia 50: 2538-2548.
13. Danober L, Deransart C, Depaulis A, Vergnes M, Marescaux C, (1998) Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55: 27-57.
14. Depaulis A, van Luijtelaar G (2006) Genetics models of Absence Epilepsy in the rat. In: Schwartzkroin PA, Pitkanen A, Moshé SL, editors. Models of Seizures and Epilepsy. London: Elsevier Academic Press. 233-248.
15. Meeren HK, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH, (2002) Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 22: 1480-1495.
16. Meeren H, van Luijtelaar G, Lopes da Silva F, Coenen A, (2005) Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Arch Neurol 62: 371-376.
17. Polack PO, Guillemain I, Hu E, Deransart C, Depaulis A, et al. (2007) Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27: 6590-6599.
18. David O, Guillemain I, Saillet S, Reyt S, Deransart C, et al. (2008) Identifying neural drivers with functional MRI: an electrophysiological validation. PLoS Biol 6: 2683-2697.
19. Polack PO, Mahon S, Chavez M, Charpier S, (2009) Inactivation of the somatosensory cortex prevents paroxysmal oscillations in cortical and related thalamic neurons in a genetic model of absence epilepsy. Cereb Cortex 19: 2078-2091.
20. Chipaux M, Charpier S, Polack PO, (2011) Chloride-mediated inhibition of the ictogenic neurones initiating genetically-determined absence seizures. Neuroscience 192: 642-651.
21. Timofeev I, Steriade M, (2004) Neocortical seizures: initiation, development and cessation. Neuroscience 123: 299-336.
22. Paz J, Polack PO, Slaght SJ, Deniau JM, Chavez M, et al. (2009) Cortical initiation of absence seizures, propagation to basal ganglia and back to the cortex. In: Tang FR, editor. Pan-brain abnormal neural network in epilepsy. Kerala: Research Signpost. 41-65.
23. Schwab R, (1939) A method of measuring consciousness in petit mal epilepsy. J Nerv Ment Dis 89: 690-691.
24. Mirsky AF, Vanburen JM, (1965) On the nature of the "absence" in centrencephalic epilepsy: a study of some behavioral electroencephalographic and autonomic factors. Electroencephalogr Clin Neurophysiol 18: 334-348.
25. Kostopoulos GK, (2001) Involvement of the thalamocortical system in epileptic loss of consciousness. Epilepsia 42 (Suppl 3): 13-19.
26. Blumenfeld H, Taylor J, (2003) Why do seizures cause loss of consciousness? Neuroscientist 9: 301-310.
27. Jung R, (1939) Uber vegetative Reaktionen und Hemmungswirkung von Sinnesreizen im kleinen epileptischen Anfall. Nervenarzt 12: 169-185.
28. Fedio P, Mirsky AF, (1969) Selective intellectual deficits in children with temporal lobe or centrencephalic epilepsy. Neuropsychologia 7: 287-300.
29. Duncan C (1988) Application of event-related brain potentials to the analysis of interictal attention in absence epilepsy. In: Myslobodsky MS, Mirsky AF, editors. Elements of Petit Mal Epilepsy. New York: Peter Lang. 341-364.
30. Duncan CC, Mirsky AF, Lovelace CT, Theodore WH, (2009) Assessment of the attention impairment in absence epilepsy: comparison of visual and auditory P300. Int J Psychophysiol 73: 118-122.
31. Orren MM (1978) Evoked potential studies in petit mal epilepsy. Visual information processing in relation to spike and wave discharges. Electroencephalogr Clin Neurophysiol Suppl 34: 251-257.
32. Blumenfeld H, Westerveld M, Ostroff RB, Vanderhill SD, Freeman J, et al. (2003) Selective frontal, parietal, and temporal networks in generalized seizures. Neuroimage 19: 1556-1566.
33. van Luijtelaar G, Sitnikova E, (2006) Global and focal aspects of absence epilepsy: the contribution of genetic models. Neurosci Biobehav Rev 30: 983-1003.
34. Polack PO, Charpier S, (2009) Ethosuximide converts ictogenic neurons initiating absence seizures into normal neurons in a genetic model. Epilepsia 50: 1816-1820.
35. Vergnes M, Marescaux C, Boehrer A, Depaulis A, (1991) Are rats with genetic absence epilepsy behaviorally impaired? Epilepsy Res 9: 97-104.
36. Getova D, Bowery NG, Spassov V, (1997) Effects of GABAB receptor antagonists on learning and memory retention in a rat model of absence epilepsy. Eur J Pharmacol 320: 9-13.
37. Pastor MA, Valencia M, Artieda J, Alegre M, Masdeu JC, (2007) Topography of cortical activation differs for fundamental and harmonic frequencies of the steady-state visual-evoked responses. An EEG and PET H215O study. Cereb Cortex 17: 1899-1905.
38. Vialatte FB, Maurice M, Dauwels J, Cichocki A, (2010) Steady-state visually evoked potentials: focus on essential paradigms and future perspectives. Prog Neurobiol 90: 418-438.
39. Pidoux M, Mahon S, Deniau JM, Charpier S, (2011) Integration and propagation of somatosensory responses in the corticostriatal pathway: an intracellular study in vivo. J Physiol 589: 263-281.
40. Commission on classification and terminology of the ILAE (1989) Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 30: 389-399.
41. Hirsch E, Panayiotopoulos CP (2005) Epilepsie-absences de l'enfance et syndromes apparentés. In: Bureau M, Roger J, Dravet C, Genton P, Tassinari CA, et al., editors. Les syndromes épileptiques de l'enfant et de l'adolescent. London: John Libbey. 315-336.
42. Jasper H, (1958) Report of the committee on methods of clinical examination in electroenchephalography. Electroencephalogr Clin Neurophysiol 10: 370-375.
43. Rees G, Kreiman G, Koch C, (2002) Neural correlates of consciousness in humans. Nat Rev Neurosci 3: 261-270.
44. Bruno RM, Sakmann B, (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312: 1622-1627.
45. Paxinos G, Watson C (1986) The brain in stereotaxic coordinates. Sydney: Academic Press. 456 p.
46. Chung S, Li X, Nelson SB, (2002) Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34: 437-446.
47. Carvell GE, Simons DJ, (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638-2648.
48. Fox K (2008) Barrel cortex. Cambridge: Cambridge University Press. 298 p.
49. Mahon S, Deniau JM, Charpier S, (2003) Various synaptic activities and firing patterns in cortico-striatal and striatal neurons in vivo. J Physiol Paris 97: 557-566.
50. Mahon S, Charpier S, (2012) Bidirectional plasticity of intrinsic excitability controls sensory inputs efficiency in layer 5 barrel cortex neurons in vivo. J Neurosci 32: 11377-11389.
51. Syed E, Sharott A, Moll CK, Engel AK, Kral A, (2011) Effect of sensory stimulation in rat barrel cortex, dorsolateral striatum and on corticostriatal functional connectivity. Eur J Neurosci 33: 461-470.
52. Manning JP, Richards DA, Leresche N, Crunelli V, Bowery NG, (2004) Cortical-area specific block of genetically determined absence seizures by ethosuximide. Neuroscience 123: 5-9.
53. Gutnick M, Crill WE (1995) The cortical neuron as an electrophysiological unit. In Gutnick MJ, Mody I editors. The Cortical Neuron. Oxford: Oxford University Press. 33-52.
54. Nicolelis MA, Fanselow EE, (2002) Thalamocortical optimization of tactile processing according to behavioral state. Nat Neurosci 5: 517-523.
55. Conte B, Cutrufo C, Manzini S, (1996) Electrocorticographic desynchronization after application of visceral and somatic noxious stimuli in urethane-anesthetized rats: effect of intrathecal administration of tachykinin (NK 1 or NK 2) receptor antagonists. J Pharmacol Exp Ther 276: 212-218.
56. Simons D, Carvell GE, Hershey AE, Bryant DP, (1992) Responses of barrel cortex neurons in awake rats and effects of urethane anesthesia. Exp Brain Res 91: 259-272.
57. Steriade M, McCormick DA, Sejnowski TJ, (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.
58. Steriade M, (2000) Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101: 243-276.
59. Llinas RR, Steriade M, (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95: 3297-3308.
60. Pinault D, Leresche N, Charpier S, Deniau JM, Marescaux C, et al. (1998) Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy. J Physiol 509: 449-456.
61. Slaght SJ, Paz T, Mahon S, Maurice N, Charpier S, et al. (2002) Functional organization of the circuits connecting the cerebral cortex and the basal ganglia: implications for the role of the basal ganglia in epilepsy. Epileptic Disord 4 (Suppl 3): S9-22.
62. Pinault D, (2003) Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations. J Physiol 552: 881-905.
63. Brecht M, Sakmann B, (2002) Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol 538: 495-515.
64. Wiest M, Nicolelis MA, (2003) Behavioral detection of tactile stimuli during 7-12 Hz cortical oscillations in awake rats. Nat Neurosci 6: 913-914.
65. Shaw F, (2004) Is spontaneous high-voltage rhythmic spike discharge in Long Evans rats an absence-like seizure activity? J Neurophysiol 9: 63-77.
66. Polack PO, Charpier S, (2006) Intracellular activity of cortical and thalamic neurones during high-voltage rhythmic spike discharge in Long-Evans rats in vivo. J Physiol 571: 461-476.
67. Charpier S, Leresche N, Deniau JM, Mahon S, Hughes SW, et al. (1999) On the putative contribution of GABA(B) receptors to the electrical events occurring during spontaneous spike and wave discharges. Neuropharmacology 38: 1699-1706.
68. Azouz R, Gray CM, (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209-2223.
69. Steriade M, Dossi RC, Nuñez A, (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. J Neurosci 11: 3200-3217.
70. Young G, Pigott SE, (1999) Neurobiological basis of consciousness. Arch Neurol 56: 153-157.
71. Edeline J, (2003) The thalamo-cortical auditory receptive fields: Regulation by the states of vigilance, learning and the neuromodulatory systems. Exp Brain Res 153: 554-572.
72. Bastuji H, García-Larrea L, (1999) Evoked potentials as a tool for the investigation of human sleep. Sleep Med Rev 3: 23-45.
73. Portas C, Krakow K, Allen P, Josephs O, Armony JL, et al. (2000) Auditory processing across the sleep-wake cycle: Simultaneous EEG and fMRI monitoring in humans. Neuron 28: 991-999.
74. Wygnanski-Jaffe T, Panton CM, Buncic JR, Westall CA, (2009) Paradoxical robust visual evoked potentials in young patients with cortical blindness. Doc Ophthalmol 119: 101-107.
75. Dang-Vu TT, Bonjean M, Schabus M, Boly M, Darsaud A, et al. (2011) Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc Natl Acad Sci USA 108: 15438-15443.
76. Schabus M, Dang-Vu TT, Heib DP, Boly M, Desseilles M, et al. (2012) The Fate of Incoming Stimuli during NREM Sleep is Determined by Spindles and the Phase of the Slow Oscillation. Front Neurol 3: 40.
77. Massimini M, Rosanova M, Mariotti M, (2003) EEG slow (approximately 1 Hz) waves are associated with non stationarity of thalamocortical sensory processing in the sleeping human. J Neurophysiol 89: 1205-1213.
78. Libet B, Alberts WW, Wright EW Jr, Feinstein B, (1967) Responses of human somatosensory cortex to stimuli below threshold for conscious sensation. Science 158: 1597-1600.
79. Libet B, Alberts WW, Wright EW Jr, Feinstein B (1972) Cortical and thalamic activation in conscious sensory experience. In: Somjen GG, editor. Neurophysiology studied in man. Amsterdam: Excerpta Medica. 157-168.
80. Hamandi K, Salek-Haddadi A, Laufs H, Liston A, Friston K, et al. (2006) EEG-fMRI of idiopathic and secondarily generalized epilepsies. Neuroimage 31: 1700-1710.
81. Blumenfeld H, Varghese GI, Purcaro MJ, Motelow JE, Enev M, et al. (2009) Cortical and subcortical networks in human secondarily generalized tonic-clonic seizures. Brain 132: 999-1012.