Spatiotemporal dynamics of optogenetically induced and spontaneous seizure transitions in primary generalized epilepsy

Journal of Neurophysiology

Volumn 113, Issue 7, 2015, Pages 2321-2341

  Wagner, Fabien B ^a,b   Truccolo, Wilson ^a,c,d   Wang, Jing ^b   Nurmikko, Arto V ^a,b,c  

^a BROWN UNIVERSITY   (United States)

^b Brown University   (United States)

^c BROWN UNIVERSITY   (United States)

^d DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

Absence seizures; Epilepsy; Microelectrode arrays; Optogenetics

Indexed keywords

ABSENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DYNAMICS; GENERALIZED EPILEPSY; MALE; NEOCORTEX; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; RAT; SEIZURE; SOMATOSENSORY CORTEX; SPIKE WAVE; STIMULUS RESPONSE; ANIMAL; BIOLOGICAL RHYTHM; DISEASE COURSE; ELECTROSTIMULATION; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PROCEDURES; SPATIOTEMPORAL ANALYSIS;

ANIMALS; BIOLOGICAL CLOCKS; DISEASE PROGRESSION; ELECTRIC STIMULATION; EPILEPSY, ABSENCE; EPILEPSY, GENERALIZED; MALE; NEOCORTEX; NERVE NET; OPTOGENETICS; RATS; SEIZURES; SPATIO-TEMPORAL ANALYSIS;

EID: 84940474793     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01040.2014     Document Type: Article

References (67)

1. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300, 1995.
2. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188, 2001.
3. Bernier GP, Richer F, Giard N, Bouvier G, Mercier M, Turmel A, Saint-Hilaire JM. Electrical stimulation of the human brain in epilepsy. Epilepsia 31: -513-52, 1990.
4. Blume WT, Jones DC, Pathak P. Properties of after-discharges from cortical electrical stimulation in focal epilepsies. Clin Neurophysiol 115: 982-989, 2004.
5. Blumenfeld H, McCormick DA. Corticothalamic inputs control the pattern of activity generated in thalamocortical networks. J Neurosci 20: 5153-5162, 2000.
6. Castro-Alamancos MA, Connors BW. Cellular mechanisms of the augmenting response: short-term plasticity in a thalamocortical pathway. J Neurosci 16: 7742-7756, 1996.
7. Chapin JK, Lin CS. Mapping the body representation in the SI cortex of anesthetized and awake rats. J Comp Neurol 229: 199-213, 1984.
8. Chervin RD, Pierce PA, Connors BW. Periodicity and directionality in the propagation of epileptiform discharges across neocortex. J Neurophysiol 60: 1695-1713, 1988.
9. Clasadonte J, Haydon PG. Astrocytes and epilepsy. In: Jasper’s Basic Mechanisms of the Epilepsies, edited by Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV. Bethesda, MD: National Center for Biotechnology Information, 2012, p. 591-605.
10. Coenen AML, van Luijtelaar EL. Genetic animal models for absence epilepsy: a review of the WAG/Rij strain of rats. Behav Genet 33: 635-655, 2003.
11. David O, Bastin J, Chabardès S, Minotti L, Kahane P. Studying network mechanisms using intracranial stimulation in epileptic patients. Front Syst Neurosci 4: 148, 2010.
12. B receptors. J Neurosci 18: 9099-9111, 1998.
13. Destexhe A, McCormick DA, Sejnowski TJ. Thalamic and thalamocortical mechanisms underlying 3 Hz spike-and-wave discharges. Prog Brain Res 121: 289-307, 1999.
14. Diester I, Kaufman MT, Mogri M, Pashaie R, Goo W, Yizhar O, Ramakrishnan C, Deisseroth K, Shenoy KV. An optogenetic toolbox designed for primates. Nat Neurosci 14: 387-397, 2011.
15. Elwassif MM, Kong Q, Vazquez M, Bikson M. Bio-heat transfer model of deep brain stimulation induced temperature changes. Conf Proc IEEE Eng Med Biol Soc 1: 3580-3583, 2006.
16. Ferrie CD. Idiopathic generalized epilepsies imitating focal epilepsies. Epilepsia 46: 91-95, 2005.
17. Fujita S, Adachi K, Koshikawa N, Kobayashi M. Spatiotemporal dynamics of excitation in rat insular cortex: intrinsic corticocortical circuit regulates caudal-rostro excitatory propagation from the insular to frontal cortex. Neuroscience 165: 278-292, 2010.
18. Guerrini R, Genton P. Epileptic syndromes and visually induced seizures. Epilepsia 45: 14-18, 2004.
19. Gurbanova AA, Aker R, Berkman K, Onat FY, Rijn CM, van Luijtelaar G. Effect of systemic and intracortical administration of phenytoin in two genetic models of absence epilepsy. Br J Pharmacol 148: 1076-1082, 2006.
20. Hastie T, Tibshirani R, Friedman J. The Elements of Statistical Learning: Data Mining and Prediction. New York: Springer Science & Business Media, 2009.
21. Histed MH, Bonin V, Reid RC. Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 63: 508-522, 2009.
22. Holmes MD, Brown M, Tucker DM. Are "generalized" seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 45: 1568-1579, 2004.
23. Horn BK, Schunck BG. Determining optical flow. In: SPIE 1981 Technical Symposium East. Washington, DC: International Society for Optics and Photonics, 1981, p. 319-331.
24. Jandó G, Carpi D, Kandel A, Urioste R, Horvath Z, Pierre E, Vadi D, Vadasz C, Buzsáki G. Spike-and-wave epilepsy in rats: sex differences and inheritance of physiological traits. Neuroscience 64: 301-317, 1995.
25. Jirsa VK, Stacey WC, Quilichini PP, Ivanov AI, Bernard C. On the nature of seizure dynamics. Brain 137: 2210-2230, 2014.
26. Kalamangalam GP, Tandon N, Slater JD. Dynamic mechanisms underlying afterdischarge: a human subdural recording study. Clin Neurophysiol 125: 1324-1338, 2014.
27. Kalitzin SN, Velis DN, Lopes da Silva FH. Stimulation-based anticipation and control of state transitions in the epileptic brain. Epilepsy Behav 17: 310-323, 2010.
28. Klein JP, Khera DS, Nersesyan H, Kimchi EY, Waxman SG, Blumenfeld H. Dysregulation of sodium channel expression in cortical neurons in a rodent model of absence epilepsy. Brain Res 1000: 102-109, 2004.
29. Krook-Magnuson E, Armstrong C, Oijala M, Soltesz I. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat Commun 4: 1376, 2013.
30. Lefèvre J, Baillet S. Optical flow approaches to the identification of brain dynamics. Hum Brain Mapp 30: 1887-1897, 2009.
31. Lombroso CT. Consistent EEG focalities detected in subjects with primary generalized epilepsies monitored for two decades. Epilepsia 38: 797-812, 1997.
32. Lüttjohann A, Zhang S, de Peijper R, van Luijtelaar G. Electrical stimulation of the epileptic focus in absence epileptic WAG/Rij rats: assessment of local and network excitability. Neuroscience 188: 125-134, 2011.
33. Mares P, Tolmacheva E. Comparison of cortical epileptic afterdischarges in immature genetic absence epilepsy WAG/Rij rats with those in two other strains (ACI and Wistar). Epilepsia 48: 164-167, 2007.
34. Meeren HK, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH. Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 22: 1480-1495, 2002.
35. Menzer DL, Bokil H, Ryou JW, Schiff ND, Purpura KP, Mitra PP. Characterization of trial-to-trial fluctuations in local field potentials recorded in cerebral cortex of awake behaving macaque. J Neurosci Methods 186: 250-261, 2010.
36. Mitra P, Bokil H. Observed Brain Dynamics (1st ed.). Oxford: Oxford University Press, 2007.
37. Mohajerani MH, Chan AW, Mohsenvand M, LeDue J, Liu R, McVea DA, Boyd JD, Wang YT, Reimers M, Murphy TH. Spontaneous cortical activity alternates between motifs defined by regional axonal projections. Nat Neurosci 16: 1426-1435, 2013.
38. Osawa S, Iwasaki M, Hosaka R, Matsuzaka Y, Tomita H, Ishizuka T, Sugano E, Okumura E, Yawo H, Nakasato N, Tominaga T, Mushiake H. Optogenetically induced seizure and the longitudinal hippocampal network dynamics. PLoS One 8: e60928, 2013.
39. Ozden I, Wang J, Lu Y, May T, Lee J, Goo W, O’Shea DJ, Kalanithi P, Diester I, Diagne M, Deisseroth K, Shenoy KV, Nurmikko AV. A coaxial optrode as multifunction write-read probe for optogenetic studies in nonhuman primates. J Neurosci Methods 219: 142-154, 2013.
40. Panayiotopoulos CP. The Epilepsies: Seizures, Syndromes and Management. Oxford: Bladon Medical, 2005.
41. Paz JT, Davidson TJ, Frechette ES, Delord B, Parada I, Peng K, Deisseroth K, Huguenard JR. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat Neurosci 16: 64-70, 2013.
42. Polack PO, Guillemain I, Hu E, Deransart C, Depaulis A, Charpier S. Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27: 6590-6599, 2007.
43. Polack PO, Mahon S, Chavez M, Charpier S. 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, 2009.
44. Pollen DA. Intracellular studies of cortical neurons during thalamic induced wave and spike. Electroencephalogr Clin Neurophysiol 17: 398-404, 1964.
45. Slater JD, Khan S, Li Z, Castillo E. Characterization of interictal epileptiform discharges with time-resolved cortical current maps using the helmholtz-hodge decomposition. Front Neurol 3: 138, 2012.
46. Stark E, Abeles M. Predicting movement from multiunit activity. J Neurosci 27: 8387-8394, 2007.
47. Steriade M. Interneuronal epileptic discharges related to spike-and-wave cortical seizures in behaving monkeys. Electroencephalogr Clin Neurophysiol 37: 247-263, 1974.
48. Steriade M, Oakson G, Diallo A. Cortically elicited spike-wave afterdischarges in thalamic neurons. Electroencephalogr Clin Neurophysiol 41: 641-644, 1976.
49. Steriade M, Timofeev I, Grenier F, Dürmüller N. Role of thalamic and cortical neurons in augmenting responses and self-sustained activity: dual intracellular recordings in vivo. J Neurosci 18: 6425-6443, 1998.
50. Steriade M, Yossif G. Spike-and-wave afterdischarges in cortical somatosensory neurons of cat. Electroencephalogr Clin Neurophysiol 37: 633-648, 1974.
51. Sysoeva MV, Sitnikova E, Sysoev IV, Bezruchko BP, van Luijtelaar G. Application of adaptive nonlinear Granger causality: disclosing network changes before and after absence seizure onset in a genetic rat model. J Neurosci Methods 226: 33-41, 2014.
52. Tchumatchenko T, Newman JP, Fong M, Potter SM. Delivery of continuously-varying stimuli using channelrhodopsin-2. Front Neural Circuits 7: 184, 2013.
53. Timofeev I, Grenier F, Bazhenov M, Houweling AR, Sejnowski TJ, Steriade M. Short- and medium-term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo. J Physiol 542: 583-598, 2002.
54. Topalkara K, Alarcón G, Binnie CD. Effects of flash frequency and repetition of intermittent photic stimulation on photoparoxysmal responses. Seizure 7: 249-255, 1998.
55. van Luijtelaar G, Hramov A, Sitnikova E, Koronovskii A. Spike-wave discharges in WAG/Rij rats are preceded by delta and theta precursor activity in cortex and thalamus. Clin Neurophysiol 122: 687-695, 2011.
56. Vedam-Mai V, van Battum EY, Kamphuis W, Feenstra MGP, Denys D, Reynolds BA, Okun MS, Hol EM. Deep brain stimulation and the role of astrocytes. Mol Psychiatry 17: 115, 2012.
57. Vergnes M, Marescaux C, Micheletti G, Reis J, Depaulis A, Rumbach L, Warter JM. Spontaneous paroxysmal electroclinical patterns in rat: a model of generalized non-convulsive epilepsy. Neurosci Lett 33: 97-101, 1982.
58. Wang J, Wagner F, Borton DA, Zhang J, Ozden I, Burwell RD, Nurmikko AV, van Wagenen R, Diester I, Deisseroth K. Integrated device for combined optical neuromodulation and electrical recording for chronic in vivo applications. J Neural Eng 9: 016001, 2012.
59. Wang L, Jacques SL, Zheng L. MCML-Monte Carlo modeling of light transport in multi-layered tissues. Comput Methods Programs Biomed 47: 131-146, 1995.
60. Westmijse I, Ossenblok P, Gunning B, van Luijtelaar G. Onset and propagation of spike and slow wave discharges in human absence epilepsy: a MEG study. Epilepsia 50: 2538-2548, 2009.
61. Wieser HG, Bancaud J, Talairach J, Bonis A, Szikla G. Comparative value of spontaneous and chemically and electrically induced seizures in establishing the lateralization of temporal lobe seizures. Epilepsia 20: 47-59, 1979.
62. Wykes RC, Heeroma JH, Mantoan L, Zheng K, MacDonald DC, Deisseroth K, Hashemi KS, Walker MC, Schorge S, Kullmann DM. Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy. Sci Transl Med 4: 161ra152, 2012.
63. Yaroslavsky AN, Schulze PC, Yaroslavsky IV, Schober R, Ulrich F, Schwarzmaier HJ. Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range. Phys Med Biol 47: 2059-2073, 2002.
64. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. Optogenetics in neural systems. Neuron 71: 9-34, 2011a.
65. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477: 171-178, 2011b.
66. Zangaladze A, Sharan A, Evans J, Wyeth DH, Wyeth EG, Tracy JI, Chervoneva I, Sperling MR. The effectiveness of low-frequency stimulation for mapping cortical function. Epilepsia 49: 481-487, 2008.
67. Zheng TW, O’Brien TJ, Morris MJ, Reid CA, Jovanovska V, O’Brien P, van Raay L, Gandrathi AK, Pinault D. Rhythmic neuronal activity in S2 somatosensory and insular cortices contribute to the initiation of absencerelated spike-and-wave discharges. Epilepsia 53: 1948-1958, 2012.