Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations

Journal of Neuroscience

Volumn 24, Issue 43, 2004, Pages 9658-9668

  Fisahn, André ^a,e,f   Contractor, Anis ^b   Traub, Roger D ^c   Buhl, Eberhard H ^d,e   Heinemann, Stephen F ^b   McBain, Chris J ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e MEDICAL RESEARCH COUNCIL   (United Kingdom)

^f KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Epilepsy; Gamma oscillations; Hippocampus; Interneurons; Kainate receptors; Knock out mice

Indexed keywords

ACETIC ACID; GLUTAMATE RECEPTOR 5; GLUTAMATE RECEPTOR 6; KAINIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CELL FUNCTION; CONTROLLED STUDY; DENDRITE; EPILEPSY; HIPPOCAMPUS; INTERNEURON; KNOCKOUT MOUSE; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPSE;

ANIMALS; AXONS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; HIPPOCAMPUS; INTERNEURONS; KAINIC ACID; MALE; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; OSCILLOMETRY; PROTEIN KINASE C; PYRAMIDAL CELLS; RECEPTORS, KAINIC ACID; SYNAPSES;

EID: 7444249504     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2973-04.2004     Document Type: Article

References (55)

1. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375-403.
2. Ben-Ari Y, Cossart R (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23:580-587.
3. Bortolotto ZA, Clarke VR, Delany CM, Parry MC, Smolders I, Vignes M, Ho KH, Miu P, Brinton BT, Fantaske R, Ogden A, Gates M, Ornstein PL, Lodge D, Bleakman D, Collingridge GL (1999) Kainate receptors are involved in synaptic plasticity. Nature 402:297-301.
4. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (1995) Gamma (40-100 Hz) oscillations in the hippocampus of the behaving rat. J Neurosci 15:47-60.
5. Bureau I, Bischoff S, Heinemann SF, Mulle C (1999) Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J Neurosci 19:653-663.
6. Castillo PE, Malenka RC, Nicoll RA (1997) Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388:182-186.
7. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GM, Henley JM (1996) Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379:78-81.
8. Clarke V, Ballyk B, Hoo K, Mandelzys A, Pellizzari A, Bath C, Thomas J, Sharpe E, Davies C, Ornstein P, Schoepp DD, Kamboj RK, Collingridge GL, Lodge D, Bleakman D (1997) A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389:599-603.
9. Contractor A, Swanson GT, Sailer A, O'Gorman S, Heinemann SF (2000) Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci 20:8269-8278.
10. Contractor A, Swanson GT, Heinemann SF (2001) Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29:209-216.
11. -/- mice. J Neurosci 23:422-429.
12. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y (1998) GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470-478.
13. Cossart R, Tyzio R, Dinocourt C, Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C (2001) Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29:497-508.
14. Cui C, Mayer M (1999) Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J Neurosci 19:8281-8291.
15. Fisahn A, Pike F, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
16. Fisahn A, Yamada M, Duttaroy A, Can JW, Deng CX, McBain CJ, Wess J (2002) Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33:615-624.
17. Frerking M, Ohliger-Frerking P (2002) AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22:7434-7443.
18. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479-486.
19. Frerking M, Petersen CCH, Nicoll RA (1999) Mechanisms underlying kainate receptor-mediated disinhibition in the hippocampus. Proc Natl Acad Sci USA 96:12917-12922.
20. Freund T, Buzsaki G (1996) Hippocampal interneurons. Hippocampus 6:347-470.
21. Gray CM, König P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334-337.
22. Hormuzdi S, Pais I, LeBeau FEN, Towers SK, Rozov A, Buhl EH, Whittington M, Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31:487-495.
23. Jiang L, Xu J, Nedergaard M, Kang J (2001) A kainate receptor increases the efficacy of GABAergic synapses. Neuron 30:503-513.
24. Khalilov I, Hirsch J, Cossart R, Ben-Ari Y (2002) Paradoxical anti-epileptic effects of a GluR5 agonist of kainate receptors. J Neurophysiol 88:523-527.
25. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618.
26. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
27. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41-47.
28. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4:481-495.
29. Lerma J, Paternain AV, Rodriguez-Moreno A, Lopez-Garcia JC (2001) Molecular physiology of kainate receptors. Physiol Rev 81:971-998.
30. Mathern GW, Pretorius JK, Kornblum HI, Mendoza D, Lozada A, Leite JP, Chimelli L, Born DE, Fried I, Sakamoto AC, Assirati JA, Peacock WJ, Ojemann GA, Adelson PD (1998) Altered hippocampal kainate-receptor mRNA levels in temporal lobe epilepsy patients. Neurobiol Dis 5:151-176.
31. Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107-114.
32. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392:601-605.
33. Mulle C, Sailer A, Swanson GT, Brana C, O'Gorman S, Bettler B, Heinemann SF (2000) Subunit composition of kainate receptors in hippocampal interneurons. Neuron 28:475-484.
34. Muller D, Nikonenko I, Jourdain P, Alberi S (2002) LTP, memory and structural plasticity. Curr Mol Med 2:605-611.
35. Nadler JV (1981) Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 29:2031-2042.
36. Prince DA (1978) Neurophysiology of epilepsy. Annu Rev Neurosci 1:395-415.
37. Rodriguez-Moreno A, Lerma J (1998) Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20:1211-1218.
38. Rodriguez-Moreno A, Herreras O, Lerma J (1997) Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19:893-901.
39. Rodriguez-Moreno A, López-Garcia JC, Lerma J (2000) Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci USA 97:1293-1298.
40. Sander T, Hildmann T, Kretz R, Furst R, Sailer U, Bauer G, Schmitz B, Beck-Mannagetta G, Wienker TF, Janz D (1997) Allelic association of juvenile absence epilepsy with a GluR5 kainate receptor gene (GRIK1) polymorphism. Am J Med Genet 74:416-421.
41. Schmitz D, Frerking M, Nicoll RA (2000) Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27:327-338.
42. Schmitz D, Mellor J, Nicoll RA (2001a) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976.
43. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermielzel R, Heinemann U, Traub RD (2001b) Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
44. Semyanov A, Kullmann DM (2001) Kainate receptor-dependent axonal depolarization and action potential initiation in interneurons. Nat Neurosci 4:718-723.
45. Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349-374.
46. Smolders I, Bortolotto ZA, Clarke VR, Warre R, Khan GM, O'Neill MJ, Ornstein PL, Bleakman D, Ogden A, Weiss B, Stables JP, Ho KH, Ebinger G, Collingridge GL, Lodge D, Michotte Y (2002) Antagonists of GLU(K5)-containing kainate receptors prevent pilocarpine-induced limbic seizures. Nat Neurosci 5:796-804.
47. Swanson GT, Gereau RW, Green T, Heinemann SF (1997) Identification of amino acid residues that control functional behavior in GluR5 and GluR6 kainate receptors. Neuron 19:913-926.
48. Teitelbaum JS, Zatorre RJ, Carpenter S, Gendron D, Evans AC, Gjedde A, Cashman NR (1990) Neurologic sequelae of domoic acid intoxication due to the ingestion of contaminated mussels. N Engl J Med 322:1781-1787.
49. Traub RD, Bibbig A, Fisahn A, LeBeau FEN, Whittington MA, Buhl EH (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by charbachol in vitro. Eur J Neurosci 12:4093-4106.
50. Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FEN, Whittington MA (2001) Gap junctions between interneuron dendrites can enhance long-range synchrony of gamma oscillations. J Neurosci 21:9478-9486.
51. Traub RD, Pais I, Bibbig A, LeBeau FEN, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA (2003) Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of gamma oscillations in the hippocampus in vitro. Proc Natl Acad Sci USA 100:1370-1374.
52. Vignes M, Collingridge GL (1997) The synaptic activation of kainate receptors. Nature 388:179-182.
53. Viskontas IV, McAndrews MP, Moscovitch M (2000) Remote episodic memory deficits in patients with unilateral temporal lobe epilepsy and excisions. J Neurosci 20:5853-5857.
54. Westbrook GL, Lothman EW (1983) Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res 273:97-109.
55. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.