Bidirectional Control of Generalized Epilepsy Networks via Rapid Real-Time Switching of Firing Mode

Neuron

Volumn 93, Issue 1, 2017, Pages 194-210

  Sorokin, Jordan M ^a,b   Davidson, Thomas J ^c   Frechette, Eric ^b   Abramian, Armen M ^b   Deisseroth, Karl ^b   Huguenard, John R ^b   Paz, Jeanne T ^c,d  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GLADSTONE INSTITUTES   (United States)

Author keywords

bursts; closed loop; electrophysiology; epilepsy; optogenetics; oscillations; SSFO; thalamocortical

Indexed keywords

ABSENCE; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; GENERALIZED EPILEPSY; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NEUROMODULATION; NONHUMAN; PHASIC FIRING; PRIORITY JOURNAL; RAT; SEIZURE; THALAMOCORTICAL TRACT; TONIC FIRING; ANIMAL; BRAIN CORTEX; CYTOLOGY; DISEASE MODEL; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAM; EPILEPSY; NERVE CELL; NERVE CELL NETWORK; NERVE TRACT; OPTOGENETICS; PATCH CLAMP TECHNIQUE; PATHOPHYSIOLOGY; PHYSIOLOGY; THALAMUS;

ANIMALS; BRAIN WAVES; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ELECTROCORTICOGRAPHY; EPILEPSY; EPILEPSY, ABSENCE; MICE; NERVE NET; NEURAL PATHWAYS; NEURONS; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; RATS; THALAMUS;

EID: 85008395308     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.11.026     Document Type: Article

References (77)

1. Adams, N.C., Lozsádi, D.A., Guillery, R.W., Complexities in the thalamocortical and corticothalamic pathways. Eur. J. Neurosci. 9 (1997), 204–209.
2. Anikeeva, P., Andalman, A.S., Witten, I., Warden, M., Goshen, I., Grosenick, L., Gunaydin, L.A., Frank, L.M., Deisseroth, K., Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15 (2011), 163–170.
3. Armstrong, C., Krook-Magnuson, E., Oijala, M., Soltesz, I., Closed-loop optogenetic intervention in mice. Nat. Protoc. 8 (2013), 1475–1493.
4. Avanzini, G., Vergnes, M., Spreafico, R., Marescaux, C., Calcium-dependent regulation of genetically determined spike and waves by the reticular thalamic nucleus of rats. Epilepsia 34 (1993), 1–7.
5. Avanzini, G., de Curtis, M., Franceschetti, S., Sancini, G., Spreafico, R., Cortical versus thalamic mechanisms underlying spike and wave discharges in GAERS. Epilepsy Res. 26 (1996), 37–44.
6. Beenhakker, M.P., Huguenard, J.R., Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy?. Neuron 62 (2009), 612–632.
7. Berényi, A., Belluscio, M., Mao, D., Buzsáki, G., Closed-loop control of epilepsy by transcranial electrical stimulation. Science 337 (2012), 735–737.
8. Buzsáki, G., Moser, E.I., Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16 (2013), 130–138.
9. Buzsáki, G., Watson, B.O., Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin. Neurosci. 14 (2012), 345–367.
10. Buzsáki, G., Bickford, R.G., Ponomareff, G., Thal, L.J., Mandel, R., Gage, F.H., Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8 (1988), 4007–4026.
11. Castro-Alamancos, M.A., Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog. Neurobiol. 74 (2004), 213–247.
12. Chmielowska, J., Carvell, G.E., Simons, D.J., Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J. Comp. Neurol. 285 (1989), 325–338.
13. Coenen, A.M., Drinkenburg, W.H., Inoue, M., van Luijtelaar, E.L., Genetic models of absence epilepsy, with emphasis on the WAG/Rij strain of rats. Epilepsy Res. 12 (1992), 75–86.
14. Contreras, D., Steriade, M., Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 15 (1995), 604–622.
15. Cope, D.W., Di Giovanni, G., Fyson, S.J., Orbán, G., Errington, A.C., Lorincz, M.L., Gould, T.M., Carter, D.A., Crunelli, V., Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat. Med. 15 (2009), 1392–1398.
16. Coulter, D.A., Huguenard, J.R., Prince, D.A., Calcium currents in rat thalamocortical relay neurones: kinetic properties of the transient, low-threshold current. J. Physiol. 414 (1989), 587–604.
17. Cox, C.L., Huguenard, J.R., Prince, D.A., Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. Proc. Natl. Acad. Sci. USA 94 (1997), 8854–8859.
18. Danober, L., Depaulis, A., Marescaux, C., Vergnes, M., Effects of cholinergic drugs on genetic absence seizures in rats. Eur. J. Pharmacol. 234 (1993), 263–268.
19. Danober, L., Deransart, C., Depaulis, A., Vergnes, M., Marescaux, C., Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog. Neurobiol. 55 (1998), 27–57.
20. de Curtis, M., Avanzini, G., Thalamic regulation of epileptic spike and wave discharges. Funct. Neurol. 9 (1994), 307–326.
21. Dreyfus, F.M., Tscherter, A., Errington, A.C., Renger, J.J., Shin, H.S., Uebele, V.N., Crunelli, V., Lambert, R.C., Leresche, N., Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window. J. Neurosci. 30 (2010), 99–109.
22. Gomora, J.C., Daud, A.N., Weiergräber, M., Perez-Reyes, E., Block of cloned human T-type calcium channels by succinimide antiepileptic drugs. Mol. Pharmacol. 60 (2001), 1121–1132.
23. Gradinaru, V., Thompson, K.R., Deisseroth, K., eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol. 36 (2008), 129–139.
24. Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., Goshen, I., Thompson, K.R., Deisseroth, K., Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141 (2010), 154–165.
25. Hasselmo, M.E., Bodelón, C., Wyble, B.P., A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14 (2002), 793–817.
26. Hirata, A., Castro-Alamancos, M.A., Neocortex network activation and deactivation states controlled by the thalamus. J. Neurophysiol. 103 (2010), 1147–1157.
27. Horikawa, K., Armstrong, W.E., A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Methods 25 (1988), 1–11.
28. Hosford, D.A., Wang, Y., Utility of the lethargic (lh/lh) mouse model of absence seizures in predicting the effects of lamotrigine, vigabatrin, tiagabine, gabapentin, and topiramate against human absence seizures. Epilepsia 38 (1997), 408–414.
29. Huguenard, J.R., Neuronal circuitry of thalamocortical epilepsy and mechanisms of antiabsence drug action. Adv. Neurol. 79 (1999), 991–999.
30. Huguenard, J.R., Block of T-Type Ca(2+) channels is an important action of Succinimide Antiabsence Drugs. Epilepsy Curr. 2 (2002), 49–52.
31. Huguenard, J.R., McCormick, D.A., Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophysiol. 68 (1992), 1373–1383.
32. Huguenard, J.R., McCormick, D.A., Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci. 30 (2007), 350–356.
33. Huguenard, J.R., Prince, D.A., Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J. Neurosci. 14 (1994), 5485–5502.
34. Jahnsen, H., Llinás, R., Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. 349 (1984), 205–226.
35. Jones, E.G., Thalamic circuitry and thalamocortical synchrony. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 (2002), 1659–1673.
36. Jones, E.G., The Thalamus. History (Lond.) 326 (2007), 419–442.
37. Kostopoulos, G.K., Spike-and-wave discharges of absence seizures as a transformation of sleep spindles: the continuing development of a hypothesis. Clin. Neurophysiol. 111:Suppl 2 (2000), S27–S38.
38. Kros, L., Rooda, O.H., De Zeeuw, C.I., Hoebeek, F.E., Controlling cerebellar output to treat refractory epilepsy. Trends Neurosci. 38 (2015), 787–799.
39. Lacey, C.J., Bryant, A., Brill, J., Huguenard, J.R., Enhanced NMDA receptor-dependent thalamic excitation and network oscillations in stargazer mice. J. Neurosci. 32 (2012), 11067–11081.
40. Leresche, N., Parri, H.R., Erdemli, G., Guyon, A., Turner, J.P., Williams, S.R., Asprodini, E., Crunelli, V., On the action of the anti-absence drug ethosuximide in the rat and cat thalamus. J. Neurosci. 18 (1998), 4842–4853.
41. Lüttjohann, A., Schoffelen, J.M., van Luijtelaar, G., Peri-ictal network dynamics of spike-wave discharges: phase and spectral characteristics. Exp. Neurol. 239 (2013), 235–247.
42. Manning, J.P.A., Richards, D.A., Leresche, N., Crunelli, V., Bowery, N.G., Cortical-area-specific block of genetically determined absence seizures by ethosuximide. Neuroscience 123 (2004), 5–9.
43. Marescaux, C., Vergnes, M., Depaulis, A., Genetic absence epilepsy in rats from Strasbourg—a review. J. Neural Transm. Suppl. 35:Suppl. (1992), 37–69.
44. McCormick, D.A., Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39 (1992), 337–388.
45. McCormick, D.A., McGinley, M.J., Salkoff, D.B., Brain state dependent activity in the cortex and thalamus. Curr. Opin. Neurobiol. 31 (2015), 133–140.
46. Meeren, H.K., Pijn, J.P., Van Luijtelaar, E.L., Coenen, A.M., Lopes da Silva, F.H., Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J. Neurosci. 22 (2002), 1480–1495.
47. Meeren, H., van Luijtelaar, G., Lopes da Silva, F., Coenen, A., Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Arch. Neurol. 62 (2005), 371–376.
48. Noebels, J.L., Qiao, X., Bronson, R.T., Spencer, C., Davisson, M.T., Stargazer: a new neurological mutant on chromosome 15 in the mouse with prolonged cortical seizures. Epilepsy Res. 7 (1990), 129–135.
49. Paralikar, K.J., Rao, C.R., Clement, R.S., New approaches to eliminating common-noise artifacts in recordings from intracortical microelectrode arrays: inter-electrode correlation and virtual referencing. J. Neurosci. Methods 181 (2009), 27–35.
50. Paz, J.T., Huguenard, J.R., Microcircuits and their interactions in epilepsy: is the focus out of focus?. Nat. Neurosci. 18 (2015), 351–359.
51. Paz, J.T., Chavez, M., Saillet, S., Deniau, J.M., Charpier, S., Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway. J. Neurosci. 27 (2007), 929–941.
52. Paz, J.T., Bryant, A.S., Peng, K., Fenno, L., Yizhar, O., Frankel, W.N., Deisseroth, K., Huguenard, J.R., A new mode of corticothalamic transmission revealed in the Gria4(-/-) model of absence epilepsy. Nat. Neurosci. 14 (2011), 1167–1173.
53. Paz, J.T., Davidson, T.J., Frechette, E.S., Delord, B., Parada, I., Peng, K., Deisseroth, K., Huguenard, J.R., Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 16 (2013), 64–70.
54. Pinault, D., Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations. J. Physiol. 552 (2003), 881–905.
55. Pinault, D., Leresche, N., Charpier, S., Deniau, J.M., Marescaux, C., Vergnes, M., Crunelli, V., Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy. J. Physiol. 509 (1998), 449–456.
56. Pinault, D., Slézia, A., Acsády, L., Corticothalamic 5-9 Hz oscillations are more pro-epileptogenic than sleep spindles in rats. J. Physiol. 574 (2006), 209–227.
57. Polack, P.-O., Charpier, S., Intracellular activity of cortical and thalamic neurones during high-voltage rhythmic spike discharge in Long-Evans rats in vivo. J. Physiol. 571 (2006), 461–476.
58. Polack, P.-O., 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 (2007), 6590–6599.
59. Polack, P.O., 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 (2009), 2078–2091.
60. Poulet, J.F.A., Fernandez, L.M., Crochet, S., Petersen, C.C., Thalamic control of cortical states. Nat. Neurosci. 15 (2012), 370–372.
61. Richards, D.A., Manning, J.P., Barnes, D., Rombola, L., Bowery, N.G., Caccia, S., Leresche, N., Crunelli, V., Targeting thalamic nuclei is not sufficient for the full anti-absence action of ethosuximide in a rat model of absence epilepsy. Epilepsy Res. 54 (2003), 97–107.
62. Sarkisova, K., van Luijtelaar, G., The WAG/Rij strain: a genetic animal model of absence epilepsy with comorbidity of depression [corrected]. Prog. Neuropsychopharmacol. Biol. Psychiatry 35 (2011), 854–876.
63. Sitnikova, E., van Luijtelaar, G., Cortical control of generalized absence seizures: effect of lidocaine applied to the somatosensory cortex in WAG/Rij rats. Brain Res. 1012 (2004), 127–137.
64. Sohal, V.S., Huntsman, M.M., Huguenard, J.R., Reciprocal inhibitory connections regulate the spatiotemporal properties of intrathalamic oscillations. J. Neurosci. 20 (2000), 1735–1745.
65. Steriade, M., Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101 (2000), 243–276.
66. Steriade, M., Contreras, D., Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. J. Neurosci. 15 (1995), 623–642.
67. Steriade, M., McCormick, D.A., Sejnowski, T.J., Thalamocortical oscillations in the sleeping and aroused brain. Science 262 (1993), 679–685.
68. Talley, E.M., Cribbs, L.L., Lee, J.H., Daud, A., Perez-Reyes, E., Bayliss, D.A., Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci. 19 (1999), 1895–1911.
69. Timofeev, I., Steriade, M., Neocortical seizures: initiation, development and cessation. Neuroscience 123 (2004), 299–336.
70. Timofeev, I., Grenier, F., Steriade, M., Spike-wave complexes and fast components of cortically generated seizures. IV. Paroxysmal fast runs in cortical and thalamic neurons. J. Neurophysiol. 80 (1998), 1495–1513.
71. Torrence, C., Compo, G.P., A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79 (1998), 61–78.
72. Tsakiridou, E., Bertollini, L., de Curtis, M., Avanzini, G., Pape, H.C., Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy. J. Neurosci. 15 (1995), 3110–3117.
73. van Luijtelaar, E.L.J.M., Coenen, A.M.L., Two types of electrocortical paroxysms in an inbred strain of rats. Neurosci. Lett. 70 (1986), 393–397.
74. van Luijtelaar, G., Sitnikova, E., Global and focal aspects of absence epilepsy: the contribution of genetic models. Neurosci. Biobehav. Rev. 30 (2006), 983–1003.
75. Vergnes, M., Marescaux, C., Cortical and thalamic lesions in rats with genetic absence epilepsy. J. Neural Transm. Suppl. 35 (1992), 71–83.
76. Yizhar, O., Fenno, L.E., Prigge, M., Schneider, F., Davidson, T.J., O'Shea, D.J., Sohal, V.S., Goshen, I., Finkelstein, J., Paz, J.T., et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477 (2011), 171–178.
77. Zhang, F., Wang, L.P., Boyden, E.S., Deisseroth, K., Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3 (2006), 785–792.