Optogenetic inhibition of chemically induced hypersynchronized bursting in mice

Neurobiology of Disease

Volumn 65, Issue , 2014, Pages 133-141

  Berglind, Fredrik ^a   Ledri, Marco ^a,d   Sørensen, Andreas Toft ^a,e   Nikitidou, Litsa ^a,d   Melis, Miriam ^a,f   Bielefeld, Pascal ^a,g   Kirik, Deniz ^b   Deisseroth, Karl ^c   Andersson, My ^a   Kokaia, Merab ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c Stanford University   (United States)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF CAGLIARI   (Italy)

^g UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Bicuculline; Epileptiform; GABA; Hippocampus; Inhibition; Mouse; NpHR; Optogenetics; Picrotoxin; Seizure

Indexed keywords

HALORHODOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; EPILEPTIC DISCHARGE; FEMALE; HIPPOCAMPUS; HYPERPOLARIZATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE; SYNAPTIC INHIBITION;

BICUCULLINE; EPILEPTIFORM; GABA; HIPPOCAMPUS; INHIBITION; MOUSE; NPHR; OPTOGENETICS; PICROTOXIN; SEIZURE;

ACTION POTENTIALS; AMINOPYRIDINES; ANALYSIS OF VARIANCE; ANIMALS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FEMALE; GABA AGENTS; GABA ANTAGONISTS; HALORHODOPSINS; KAINIC ACID; LUMINESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; NEURONS; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; STATUS EPILEPTICUS; TRANSDUCTION, GENETIC;

EID: 84894236025     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.01.015     Document Type: Article

References (42)

1. Avoli M., de Curtis M. GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity. Prog. Neurobiol. 2011, 95:104-132.
2. Bogen I.L., et al. The importance of synapsin I and II for neurotransmitter levels and vesicular storage in cholinergic, glutamatergic and GABAergic nerve terminals. Neurochem. Int. 2009, 55:13-21.
3. Cantallops I., Routtenberg A. Kainic acid induction of mossy fiber sprouting: dependence on mouse strain. Hippocampus 2000, 10:269-273.
4. Cardin J.A., et al. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat. Protoc. 2010, 5:247-254.
5. Chi Z.H., et al. Zinc transporter 3 immunohistochemical tracing of sprouting mossy fibres. Neurochem. Int. 2008, 52:1305-1309.
6. Chow B.Y., et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463:98-102.
7. de Curtis M., Avanzini G. Interictal spikes in focal epileptogenesis. Prog. Neurobiol. 2001, 63:541-567.
8. de Curtis M., et al. Cellular mechanisms underlying spontaneous interictal spikes in an acute model of focal cortical epileptogenesis. Neuroscience 1999, 88:107-117.
9. de Lanerolle N.C., et al. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res. 1989, 495:387-395.
10. Duncan J.S., et al. Adult epilepsy. Lancet 2006, 367:1087-1100.
11. Empson R.M., et al. Injection of tetanus toxin into the neocortex elicits persistent epileptiform activity but only transient impairment of GABA release. Neuroscience 1993, 57:235-239.
12. Engel J. Mesial temporal lobe epilepsy: what have we learned?. Neuroscientist 2001, 7:340-352.
13. Gradinaru V., et al. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J. Neurosci. 2007, 27:14231-14238.
14. Gradinaru V., et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141:154-165.
15. Hwa G.G., et al. Bicuculline-induced epileptogenesis in the human neocortex maintained in vitro. Exp. Brain Res. 1991, 83:329-339.
16. Isomura Y., et al. A network mechanism underlying hippocampal seizure-like synchronous oscillations. Neurosci. Res. 2008, 61:227-233.
17. Krook-Magnuson E., et al. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat. Commun. 2013, 4:1376.
18. Kumar S.S., Buckmaster P.S. Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J. Neurosci. 2006, 26:4613-4623.
19. Ledri M., et al. Altered profile of basket cell afferent synapses in hyper-excitable dentate gyrus revealed by optogenetic and two-pathway stimulations. Eur. J. Neurosci. 2012, 36:1971-1983.
20. Malmgren K., Thom M. Hippocampal sclerosis-origins and imaging. Epilepsia 2012, 53(Suppl. 4):19-33.
21. Miles R., Wong R.K. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 1983, 306:371-373.
22. Morimoto K. Seizure-triggering mechanisms in the kindling model of epilepsy: collapse of GABA-mediated inhibition and activation of NMDA receptors. Neurosci. Biobehav. Rev. 1989, 13:253-260.
23. Morimoto K., Goddard G.V. Kindling induced changes in EEG recorded during stimulation from the site of stimulation: collapse of GABA-mediated inhibition and onset of rhythmic synchronous burst. Exp. Neurol. 1986, 94:571-584.
24. Paz J.T., et al. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat. Neurosci. 2013, 16:64-70.
25. Piredda S., et al. Intracerebral site of convulsant action of bicuculline. Life Sci. 1985, 36:1295-1298.
26. Pitkänen A., et al. Models of Seizures and Epilepsy 2006, Elsevier Academic, Amsterdam; Oxford.
27. Queiroz C.M., Mello L.E. Synaptic plasticity of the CA3 commissural projection in epileptic rats: an in vivo electrophysiological study. Eur. J. Neurosci. 2007, 25:3071-3079.
28. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
29. Raimondo J.V., et al. Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat. Neurosci. 2012, 15:1102-1104.
30. Royle S.J., et al. Behavioural analysis and susceptibility to CNS injury of four inbred strains of mice. Brain Res. 1999, 816:337-349.
31. Sander J.W. The epidemiology of epilepsy revisited. Curr. Opin. Neurol. 2003, 16:165-170.
32. Santoro B., et al. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci. 2000, 20:5264-5275.
33. Siwek M., et al. Voltage-gated Ca(2+) channel mediated Ca(2+) influx in epileptogenesis. Adv. Exp. Med. Biol. 2012, 740:1219-1247.
34. Strombom U., et al. Regulation of the state of phosphorylation of specific neuronal proteins in mouse brain by in vivo administration of anesthetic and convulsant agents. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:4687-4690.
35. Tonnesen J., et al. Optogenetic control of epileptiform activity. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12162-12167.
36. Traub R.D., Jefferys J.G. Simulations of epileptiform activity in the hippocampal CA3 region in vitro. Hippocampus 1994, 4:281-285.
37. Traub R.D., et al. Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after-discharges in the guinea-pig hippocampal slice. J. Physiol. 1993, 461:525-547.
38. Veliskova J., et al. Ketamine suppresses both bicuculline- and picrotoxin-induced generalized tonic-clonic seizures during ontogenesis. Pharmacol. Biochem. Behav. 1990, 37:667-674.
39. Wieser H.G., ILAE, C.o.N.o.E. ILAE Commission Report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 2004, 45:695-714.
40. Wykes R.C., et al. Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy. Sci. Transl. Med. 2012, 4:161ra152.
41. Zhang W., Buckmaster P.S. Dysfunction of the dentate basket cell circuit in a rat model of temporal lobe epilepsy. J. Neurosci. 2009, 29:7846-7856.
42. Zhang F., et al. Multimodal fast optical interrogation of neural circuitry. Nature 2007, 446:633-639.