Pre- and post-synaptic functions of kainate receptors at glutamate and GABA synapses in the rat entorhinal cortex

Hippocampus

Volumn 22, Issue 3, 2012, Pages 555-576

  Chamberlain, Sophie E L ^a,b   Jane, David E ^b   Jones, Roland S G ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Entorhinal cortex; GABA release; Glutamate release; Kainate receptors; Oscillogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; AUTORECEPTOR; GLUTAMIC ACID; KAINIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; GABAERGIC SYSTEM; INTERNEURON; MALE; NEUROTRANSMITTER RELEASE; NONHUMAN; OSCILLATION; PATCH CLAMP; PERIODICITY; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PYRAMIDAL NERVE CELL; RAT; VOLTAGE CLAMP; WHOLE CELL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ENTORHINAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; NERVE NET; NEURAL INHIBITION; NEURONS; QUINOXALINES; RATS; RATS, WISTAR; RECEPTORS, KAINIC ACID; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84857237979     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20921     Document Type: Article

References (78)

1. Agrawal SG, Evans RH. 1986. The primary afferent depolarizing action of kainate in the rat. Br J Pharmacol 87: 345-355.
2. Ali AB. 2003. Involvement of post-synaptic kainate receptors during synaptic transmission between unitary connections in rat neocortex. Eur J Neurosci 17: 2344-2350.
3. Bartolomei F, Khalil M, Wendling F, Sontheimer A, Régis J, Ranjeva JP, Guye M, Chauvel P. 2005. Entorhinal cortex involvement in human mesial temporal lobe epilepsy: An electrophysiologic and volumetric study. Epilepsia 46: 677-687.
4. Beed PS, Salmen B, Schmitz D. 2009. GluK2-mediated excitability within the superficial layers of the entorhinal cortex. PLoS One 4: e5576.
5. Ben-Ari Y, Tremblay E, Riche D, Ghilini G, Naquet R. 1981. Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6: 1361-1391.
6. 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.
7. Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH. 2007. Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32: 1888-1902.
8. Berretta N, Jones RSG. 1996a. A comparison of spontaneous EPSCs in layer II and layer IV-V neurons of the rat entorhinal cortex in vitro. J Neurophysiol 76: 1089-1100.
9. Berretta N, Jones RSG. 1996b. Tonic facilitation of glutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex. Neuroscience 75: 339-344.
10. Bettus G, Bartolomei F, Confort-Gouny S, Guedj E, Chauvel P, Cozzone PJ, Ranjeva JP, Guye M. 2010. Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiat 81: 1147-1154.
11. Braga MFM, Aroniadou-Anderjaska V, Xie JW, Li H. 2003. Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J Neurosci 23: 442-452.
12. Breustedt J, Schmitz D. 2004. Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J Neurosci 24: 10093-10098.
13. Burwell RD. 2000. The parahippocampal region: Corticocortical connectivity. Ann N Y Acad Sci 911: 25-42.
14. Campbell SL, Mathew SS, Hablitz JJ. 2007. Pre- and postsynaptic effects of kainate on layer II/III pyramidal cells in rat neocortex. Neuropharmacology 53: 37-47.
15. Castillo PE, Malenka RC, Nicoll RA. 1997. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388: 182-186.
16. Cho K, Francis JC, Hirbec H, Dev K, Brown MW, Henley JM, Bashir ZI. 2003. Regulation of kainate receptors by protein kinase C and metabotropic glutamate receptors. J Physiol 548: 723-730.
17. Christensen JK, Varming T, Ahring PK, Jørgensen TD, Nielsen EØ. 2004. In vitro characterization of 5-carboxyl-2, 4-di-benzamidobenzoic acid (NS3763), a noncompetitive antagonist of GLUK5 receptors. J Pharmacol Exp Ther 309: 1003-1010.
18. Clarke VR, Ballyk BA, Hoo KH, Mandelzys A, Pellizzari A, Bath CP, Thomas J, Sharpe EF, Davies CH, Ornstein PL, Schoepp DD, Kamboj RK, Collingridge GL, Lodge D, Bleakman D. 1997. An hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389: 599-603.
19. Contractor A, Swanson G, Heinemann SF. 2001. Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29: 209-216.
20. Contractor A, Sailer AW, Darstein M, Maron C, Xu J, Swanson GT, Heinemann SF. 2003. Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2-/- mice. J Neurosci 23: 422-429.
21. Contreras D, Timofeev I, Steriade M. 1996. Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol 494: 251-264.
22. 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.
23. Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA. 2003. Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J Neurosci 23: 9761-9769.
24. Cunningham MO, Halliday DM, Davies CH, Traub RD, Buhl EH, Whittington MA. 2004. Coexistence of gamma and high frequency oscillations in rat medial entorhinal cortex in vitro. J Physiol 559: 347-353.
25. Cunningham MO, Pervouchine DD, Racca C, Kopell NJ, Davies CH, Jones RSG, Traub RD, Whittington MA. 2006. Neuronal metabolism governs cortical network response state. PNAS 103: 5597-5601.
26. Dargan SL, Clarke VR, Alushin GM, Sherwood JL, Nisticò R, Bortolotto ZA, Ogden AM, Bleakman D, Doherty AJ, Lodge D, Mayer ML, Fitzjohn SM, Jane DE, Collingridge GL. 2009. ACET is a highly potent and specific kainate receptor antagonist: Characterization and effects on hippocampal mossy fibre function. Neuropharmacology 56: 121-130.
27. 2+ permeability of unedited and edited versions of kainate selective glutamate receptor GluR6. PNAS 90: 755-759.
28. Fisahn A. 2005. Kainate receptors and rhythmic activity in neuronal networks: Hippocampal gamma oscillations as a tool. J Physiol 562: 65-72.
29. Frerking M, Ohliger-Frerking P. 2002. AMPA receptors and kainate receptors encode different features of afferent activity. J Neurosci 22: 7434-7443.
30. Frerking M, Schmitz D, Zhou Q, Johansen J, Nicoll RA. 2001. Kainate receptors depress excitatory synaptic transmission at CA3 -> CA1 synapses in the hippocampus via a direct presynaptic action. J Neurosci 21: 2958-2966.
31. Fukushima T, Shingai R, Ogurusu T, Ichinose M. 2003. Inhibition of willardiine-induced currents through rat GluR6/KA-2 kainate receptor channels by Zinc and other divalent cations. Neurosci Lett 349: 107-110.
32. Gómez-Isla T, Price JL, McKeel DWJr, Morris JC, Growdon JH, Hyman BT. 1996. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16: 4491-4500.
33. Hahnloser RH, Douglas RJ, Hepp K. 2002. Attentional recruitment of inter-areal recurrent networks for selective gain control. Neural Comp 14: 1669-1689.
34. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26: 4535-4345.
35. Huettner JE. 2003. Kainate receptors and synaptic transmission. Prog Neurobiol 70: 387-407.
36. Huxter JR, Zinyuk LE, Roloff EL, Clarke VR, Dolman NP, More JC, Jane DE, Collingridge GL, Muller RU. 2007. Inhibition of kainate receptors reduces the frequency of hippocampal theta oscillations. JNeurosci 27: 2212-2123.
37. Jane DE, Lodge D, Collingridge GL. 2009. Kainate receptors: Pharmacology, function and therapeutic potential. Neuropharmacology 56: 90-113.
38. Jiang L, Xu J, Nedergaard M, Kang J. 2001. A kainate receptor increases the efficacy of GABAergic synapses. Neuron 30: 503-513.
39. Jones RSG, Heinemann U. 1988. Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J Neurophysiol 59: 1476-1496.
40. Jones RSG, Heinemann U. 1989. Spontaneous activity mediated by NMDA receptors in immature rat entorhinal cortex in vitro. Neurosci Lett 104: 93-98.
41. Jones RSG, Woodhall GL. 2005. Background synaptic activity in rat entorhinal cortical neurones: Differential control of transmitter release by presynaptic receptors. J Physiol 562: 107-120.
42. Kövari E, Gold G, Herrmann FR, Canuto A, Hof PR, Bouras C, Giannakopoulos P. 2003. Lewy body densities in the entorhinal and anterior cingulate cortex predict cognitive deficits in Parkinson's disease. Acta Neuropathol 106: 83-88.
43. Kidd FL, Isaac JTR. 1999. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400: 569-573.
44. Lauri SE, Delany C, Clarke VRJ, Bortolotto ZA, Ornstein PL, Isaac JTR, Collingridge GL. 2001. Synaptic activation of a presynaptic kainate receptor facilitates AMPA receptor-mediated synaptic transmission at hippocampal mossy fibre synapses. Neuropharmacology 41: 907-915.
45. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39: 327-341.
46. Lee AK, Wilson MA. 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36: 1183-1194.
47. Lerma J. 2003. Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4: 481-495.
48. Li H, Rogawski MA. 1998. GluR5 kainate receptor mediated synaptic transmission in rat basolateral amygdala in vitro. Neuropharmacology 37: 1279-1286.
49. Li H, Chen A, Xing G, Wei ML, Rogawsi MA. 2001. Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 4: 612-620.
50. Lourenço J, Cannich A, Carta M, Coussen F, Mulle C, Marsicano G. 2010. Synaptic activation of kainate receptors gates presynaptic CB(1) signaling at GABAergic synapses. Nat Neurosci 13: 197-204.
51. McCormick DA, Shu Y, Hasenstaub A, Sanchez-Vives M, Badoual M, Bal T. 2003. Persistent cortical activity: Mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13: 1219-1231.
52. Morgan NH, Stanford IM, Woodhall GL. 2008. Modulation of network oscillatory activity and GABAergic synaptic transmission by CB1 cannabinoid receptors in the rat medial entorhinal cortex. Neural Plast 808564.
53. Pennanen C, Kivipelto M, Tuomainen S, Hartikainen P, Hänninen T, Laakso MP, Hallikainen M, Vanhanen M, Nissinen A, Helkala EL, Vainio P, Vanninen R, Partanen K, Soininen H. 2004. Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiol Aging 25: 303-310.
54. Perrais D, Pinheiro PS, Jane DE, Mulle C. 2009. Antagonism of recombinant and native GluK3-containing kainate receptors. Neuropharmacology 56: 131-140.
55. Pinheiro P, Mulle C. 2006. Kainate receptors. Cell Tissue Res 326: 457-482.
56. Pinheiro PS, Perrais D, Coussen F, Barhanin J, Bettler B, Mann JR, Malva JO, Heinemann SF, Mulle C. 2007. GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 104: 12181-12186.
57. Prasad KM, Patel AR, Muddasani S, Sweeney J, Keshavan MS. 2004. The entorhinal cortex in first-episode psychotic disorders: A structural magnetic resonance imaging study. Am J Psychiat 161: 1612-1619.
58. Rodriguez Moreno A, Herreras O, Lerma J. 1997. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19: 893-901.
59. Ruano D, Lambolez B, Rossier J, Paternain AV, Lerma J. 1995. Kainate receptor subunit expressed in a single cultured hippocampal neurons: Molecular and functional variants by RNA editing. Neuron 14: 1009-1017.
60. Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034.
61. Schmitz D, Mellor J, Nicoll RA. 2001a. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291: 1972-1976.
62. Schmitz D, Mellor J, Frerking M, Nicoll RA. 2001b. Presynaptic kainate receptors at hippocampal mossy fiber synapses. PNAS 98: 11003-11008.
63. Stanger HL, Alford R, Jane DE, Cunningham MO. 2008. The role of GLU K5-containing kainate receptors in entorhinal cortex gamma frequency oscillations. Neural Plast 401645.
64. Steriade M. 2003. Neuronal Substrates of Sleep and Epilepsy. Cambridge: Cambridge University Press.
65. Steriade M, Nuñez A, Amzica F. 1993. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13: 3266-3283.
66. Shu Y, Hasenstaub A, McCormick DA. 2003. Turning on and off recurrent balanced cortical activity. Nature 423: 288-293.
67. Van Hoesen GW, Hyman BT, Damasio AR. 1991. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus 1: 1-8.
68. Vignes M, Collingridge GL. 1997. The synaptic activation of kainate receptors. Nature 388: 179-182.
69. Vincent P, Mulle C. 2009. Kainate receptors in epilepsy and excitotoxicity. Neuroscience 158: 309-323.
70. Wu LJ, Zhao MG, Toyoda H, Ko SW, Zhuo M. 2005. Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 94: 1805-1813.
71. West PJ, Dalpé-Charron A, Wilcox KS. 2007. Differential contribution of kainate receptors to excitatory post-synaptic currents in the superficial layer neurons of the rat medial entorhinal cortex. Neuroscience 146: 1000-1012.
72. Witter MP, Moser EI. 2006. Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci 29: 671-678.
73. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. 1989. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33: 161-253.
74. Wong AY, Fay AM, Bowie D. 2006. External ions are coactivators of kainate receptors. J Neurosci 26: 5750-5755.
75. Woodhall GL, Evans DIP, Cunningham MO, Jones RSG. 2001. NR2B-containing NMDA autoreceptors at synapses on entorhinal cortical neurons. J Neurophysiol 86: 1644-1651.
76. Woodhall GL, Ayman G, Jones RSG. 2007. Differential control of two forms of glutamate release by group III metabotropic glutamate receptors at rat entorhinal synapses. Neuroscience 148: 7-21.
77. Yang J, Woodhall GL, Jones RSG. 2006. Tonic facilitation of glutamate release by presynaptic NR2B-containing NMDA receptors is increased in the entorhinal cortex of chronically epileptic rats. J Neurosci 26: 406-410.
78. Yang J, Chamberlain SEL, Woodhall GL, Jones RSG. 2008. Mobility of NMDA autoreceptors but not postsynaptic receptors at glutamate synapses in the rat entorhinal cortex. J Physiol 586: 4905-4924.