Long-term depression of synaptic kainate receptors reduces excitability by relieving inhibition of the slow afterhyperpolarization

Journal of Neuroscience

Volumn 33, Issue 22, 2013, Pages 9536-9545

  Chamberlain, Sophie E L ^a   Sadowski, Josef H L P ^a   Teles Grilo Ruivo, Leonor M ^a   Atherton, Laura A ^a   Mellor, Jack R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A2A RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; HIPPOCAMPUS; MALE; MOSSY FIBER; NERVE CELL; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SPIKE; SYNAPTIC TRANSMISSION;

ANIMALS; CA3 REGION, HIPPOCAMPAL; DATA INTERPRETATION, STATISTICAL; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY POSTSYNAPTIC POTENTIALS; MALE; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTOR, ADENOSINE A2A; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84878274280     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0034-13.2013     Document Type: Article

References (44)

1. 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. CrossRef Medline
2. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR (2010) Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 68:948-963. CrossRef Medline
3. Castillo PE, Malenka RC, NicollRA (1997) Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388:182-186. CrossRef Medline
4. Chamberlain SE, González-Gonzalez IM, Wilkinson KA, Konopacki FA, Kantamneni S, Henley JM, Mellor JR (2012) SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat Neurosci 15:845-852. CrossRef Medline
5. Cherubini E, Rovira C, Ben-Ari Y, Nistri A (1990) Effects of kainate on the excitability of rat hippocampal neurones. Epilepsy Res 5:18-27. CrossRef Medline
6. 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. CrossRef Medline
7. Darstein M, Petralia RS, Swanson GT, Wenthold RJ, Heinemann SF (2003) Distribution of Kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23:8013-8019. Medline
8. Fernandes HB, Catches JS, Petralia RS, Copits BA, Xu J, Russell TA, Swanson GT, Contractor A (2009) High-affinity kainate receptor subunits are necessary for ionotropic but not metabotropic signaling. Neuron 63:818-829. CrossRef Medline
9. Fernández de Sevilla D, Fuenzalida M, Porto Pazos AB, Buño W (2007) Selective shunting of the NMDA EPSP component by the slow afterhyperpolarization in rat CA1 pyramidal neurons. J Neurophysiol 97: 3242-3255. CrossRef Medline
10. Fisahn A, Heinemann SF, McBain CJ (2005) The Kainate receptor subunit GluR6 mediates metabotropic regulation of the slow and medium AHP currents in mouse hippocampal neurones. J Physiol 562:199-203. CrossRef Medline
11. Frerking M, Ohliger-Frerking P (2002) AMPA receptors and Kainate receptors encode different features of afferent activity. J Neurosci 22:7434-7443. Medline
12. 2+)/calmodulindependent protein kinase. J Neurosci 20:2766-2773. Medline
13. Gundlfinger A, Breustedt J, Sullivan D, Schmitz D (2010) Natural spike trains trigger short-and long-lasting dynamics at hippocampal mossy fiber synapses in rodents. PLoS ONE 5:e9961. CrossRef Medline
14. Ito K, Contractor A, Swanson GT (2004) Attenuated plasticity of postsynaptic kainite receptors in hippocampal CA3 pyramidal neurons. J Neurosci 24:6228-6236. CrossRef Medline
15. Kamiya H, Shinozaki H, Yamamoto C (1996) Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J Physiol 493:447-455. Medline
16. 2++ influx at the hippocampal mossy fiber synapses. J Neurosci 22:9237-9243. Medline
17. Kwon HB, Castillo PE (2008a) Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron 57: 108-120. CrossRef Medline
18. Kwon HB, Castillo PE (2008b) Role of glutamate autoreceptors at hippocampal mossy fiber synapses. Neuron 60:1082-1094. CrossRef Medline
19. Lei S, Pelkey KA, Topolnik L, Congar P, Lacaille JC, McBain CJ (2003) Depolarization-induced long-term depression at hippocampal mossy fiber-CA3 pyramidal neuron synapses. J Neurosci 23:9786-9795. Medline
20. Martin S, Nishimune A, Mellor JR, Henley JM (2007) SUMOylation regulates kainate-receptor-mediated synaptic transmission. Nature 447:321-325. CrossRef Medline
21. Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107-114. CrossRef Medline
22. Melyan Z, Lancaster B, Wheal HV (2004) Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 24:4530-4534. CrossRef Medline
23. Mistry R, Dennis S, Frerking M, Mellor JR (2011) Dentate gyrus granule cell firing patterns can induce mossy fiber long-term potentiation in vitro. Hippocampus 21:1157-1168. CrossRef Medline
24. Mulle C, Sailer A, Pérez-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. CrossRef Medline
25. Nicoll RA, SchmitzD (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6:863-876. CrossRef Medline
26. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11:1023-1035. CrossRef Medline
27. Perrais D, Pinheiro PS, Jane DE, Mulle C (2009) Antagonism of recombinant and native GluK3-containing kainate receptors. Neuropharmacology 56:131-140. CrossRef Medline
28. Pinheiro PS, Mulle C (2008) Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9:423-436. CrossRef Medline
29. Podlogar M, DietrichD (2006) Firing pattern of rat hippocampal neurons: a perforated patch-clamp study. Brain Res 1085:95-101. CrossRef Medline
30. Rebola N, Sachidhanandam S, Perrais D, Cunha RA, Mulle C (2007) Shortterm plasticity of kainate receptor-mediated EPSCs induced by NMDA receptors at hippocampal mossy fiber synapses. J Neurosci 27:3987-3993. CrossRef Medline
31. Rebola N, Lujan R, Cunha RA, MulleC (2008) Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron 57:121-134. CrossRef Medline
32. Rebola N, Carta M, Lanore F, Blanchet C, Mulle C (2011) NMDA receptordependent metaplasticity at hippocampal mossy fiber synapses. Nat Neurosci 14:691-693. CrossRef Medline
33. Ruiz A, Sachidhanandam S, Utvik JK, Coussen F, Mulle C (2005) Distinct subunits in heteromeric kainate receptors mediate ionotropic and metabotropic function at hippocampal mossy fiber synapses. J Neurosci 25:11710-11718. CrossRef Medline
34. Sachidhanandam S, Blanchet C, Jeantet Y, Cho YH, Mulle C (2009) Kainate receptors act as conditional amplifiers of spike transmission at hippocampal mossy fiber synapses. J Neurosci 29:5000-5008. CrossRef Medline
35. Schmitz D, Mellor J, Nicoll RA (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976. CrossRef Medline
36. Schmitz D, Mellor J, Breustedt J, Nicoll RA (2003) Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber longterm potentiation. Nat Neurosci 6:1058-1063. CrossRef Medline
37. Segerstråle M, Juuri J, Lanore F, Piepponen P, Lauri SE, Mulle C, Taira T (2010) High firing rate of neonatal hippocampal interneurons is caused by attenuation of afterhyperpolarizing potassium currents by tonically active kainate receptors. J Neurosci 30:6507-6514. CrossRef Medline
38. Selak S, Paternain AV, Aller IM, Picó E, Rivera R, Lerma J (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63:357-371. CrossRef Medline
39. Straub C, Hunt DL, Yamasaki M, Kim KS, Watanabe M, Castillo PE, Tomita S (2011) Distinct functions of kainate receptors in the brain are determined by the auxiliary subunit Neto1. Nat Neurosci 14:866-873. CrossRef Medline
40. Vignes M, Collingridge GL (1997) The synaptic activation of kainate receptors. Nature 388:179-182. CrossRef Medline
41. Wiebe SP, Stäubli UV (1999) Dynamic filtering of recognition memory codes in the hippocampus. J Neurosci 19:10562-10574. Medline
42. Wiebe SP, Staubli UV (2001) Recognition memory correlates of hippocampal theta cells. J Neurosci 21:3955-3967. Medline
43. Wu WW, Chan CS, Disterhoft JF (2004) Slow afterhyperpolarization governs the development of NMDA receptor-dependent afterdepolarization in CA1 pyramidal neurons during synaptic stimulation. J Neurophysiol 92:2346-2356. CrossRef Medline
44. Zaitsev AV, Anwyl R (2012) Inhibition of the slow afterhyperpolarization restores the classical spike timing-dependent plasticity rule obeyed in layer 2/3 pyramidal cells of the prefrontal cortex. J Neurophysiol 107:205-215. CrossRef Medline