Summary
Kainate receptors (KARs) effect depression of glutamate release at hippocampal mossy fiber-CA3 (MF-CA3) synapses by a metabotropic action involving adenylyl cyclase (AC) inhibition, cAMP reduction, and diminished protein kinase A (PKA) activation. Using hippocampal slices, we show here that KAR activation interferes with the depression of glutamate release produced by Group II metabotropic glutamate receptor stimulation and low frequency stimulation (LFS)-induced long-term depression (LTD), also expressed through presynaptic AC/cAMP/PKA at MF-CA3 synapses. The mutual occlusion of depression mediated by presynaptic KARs, Group II mGluR and LFS-induced LTD suggests their mechanistic convergence at the MF-CA3 synapse and thus invokes KARs in synaptic plasticity manifest in LTD.
Similar content being viewed by others
References
R Anwyl (1999) ArticleTitleMetabotropic glutamate receptors: electrophysiological properties and role in plasticity Brain Res Rev 29 83–120 Occurrence Handle9974152 Occurrence Handle10.1016/S0165-0173(98)00050-2 Occurrence Handle1:CAS:528:DyaK1MXhtFSjsLg%3D
ZA Bortolotto VR Clarke CM Delany MC Parry I Smolders M Vignes KH Ho P Miu BT Brinton R Fantaske A Odgen M Gates PL Ornstein D Lodge D Bleakman GL Collingridge (1999) ArticleTitleKainate receptors are involved in synaptic plasticity Nature 402 297–301 Occurrence Handle10580501 Occurrence Handle10.1038/46290 Occurrence Handle1:CAS:528:DyaK1MXnvFShs7Y%3D
PE Castillo RC Malenka RA Nicoll (1997) ArticleTitleKainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons Nature 388 182–186 Occurrence Handle9217159 Occurrence Handle10.1038/40645 Occurrence Handle1:CAS:528:DyaK2sXksFWlsLo%3D
PJ Conn JP Pin (1997) ArticleTitlePharmacology and functions of metabotropic glutamate receptors Ann Rev Pharmacol Toxicol 37 205–237 Occurrence Handle10.1146/annurev.pharmtox.37.1.205 Occurrence Handle1:CAS:528:DyaK2sXisl2ktr0%3D
A Contractor GT Swanson A Sailer S O’Gorman SF Heinemann (2000) ArticleTitleIdentification of the kainate receptors subunit underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus J Neurosci 20 8269–8278 Occurrence Handle11069933 Occurrence Handle1:CAS:528:DC%2BD3cXot1Grurw%3D
A Contractor GT Swanson SF Heinemann (2001) ArticleTitleKainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus Neuron 29 209–216 Occurrence Handle11182092 Occurrence Handle10.1016/S0896-6273(01)00191-X Occurrence Handle1:CAS:528:DC%2BD3MXisleisb8%3D
A De Blasi PJ Conn JP Pin F Nicoletti (2001) ArticleTitleMolecular determinant of metabotropic glutamate receptor signaling Trends Pharmacol Sci 22 114–120 Occurrence Handle11239574 Occurrence Handle10.1016/S0165-6147(00)01635-7 Occurrence Handle1:CAS:528:DC%2BD3MXhsVKksLw%3D
Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 479–486
LQ Huang MJ Rowan R Anwyl (1997) ArticleTitlemGluRII agonist inhibition of LTP induction: and mGluRII antagonist inhibition of LTD induction in the dentate girus in vitro NeuroRep 8 687–693 Occurrence Handle1:CAS:528:DyaK2sXisVKksrw%3D Occurrence Handle10.1097/00001756-199702100-00022
JE Huettner (2003) ArticleTitleKainate receptors and synaptic transmission Prog Neurobiol 70 387–407 Occurrence Handle14511698 Occurrence Handle10.1016/S0301-0082(03)00122-9 Occurrence Handle1:CAS:528:DC%2BD3sXnsVWltLw%3D
H Kamiya H Shinozaki C Yamamoto (1996) ArticleTitleActivation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses J Physiol 493 447–455 Occurrence Handle8782108 Occurrence Handle1:CAS:528:DyaK28XjslWns7k%3D
H Kamiya S Ozawa (2000) ArticleTitleKainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse J Physiol 523 653–665 Occurrence Handle10718745 Occurrence Handle10.1111/j.1469-7793.2000.t01-1-00653.x Occurrence Handle1:CAS:528:DC%2BD3cXitlCksr0%3D
A Kapur MF Yeckel R Gray D Johnston (1998) ArticleTitleL-type calcium channels are required for one form of hippocampal mossy fiber LTP J Neurophysiol 79 2181–2190 Occurrence Handle9535977 Occurrence Handle1:CAS:528:DyaK1cXjtVCqt70%3D
K Kobayashi T Manabe T Takahashi (1996) ArticleTitlePresynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse Science 273 648–650 Occurrence Handle8662556 Occurrence Handle10.1126/science.273.5275.648 Occurrence Handle1:CAS:528:DyaK28Xks1yntb4%3D
SE Lauri ZA Bortolotto D Bleakman PL Ornstein D Lodge JT Isaac GL Collingridge (2001a) ArticleTitleA critical role of a facilitatory presynaptic kainate receptors in mossy-fiber LTP Neuron 32 697–709 Occurrence Handle10.1016/S0896-6273(01)00511-6 Occurrence Handle1:CAS:528:DC%2BD3MXovFOis7c%3D
SE Lauri C Delany VEJ Clarke ZA Bortolotto PL Ornstein JT Isaac GL Collingridge (2001b) ArticleTitleSynaptic activation of a presynaptic kainate receptor facilitates AMPA receptor-mediated synaptic transmission at hippocampal mossy fibre synapses Neuropharmacology 41 907–915 Occurrence Handle10.1016/S0028-3908(01)00152-6 Occurrence Handle1:CAS:528:DC%2BD3MXpt1aitbc%3D
J Lerma (2003) ArticleTitleRoles and rules of kainate receptors in synaptic transmission Nat Rev Neurosci 4 481–495 Occurrence Handle12778120 Occurrence Handle10.1038/nrn1118 Occurrence Handle1:CAS:528:DC%2BD3sXktFOgtLc%3D
JV Negrete-Díaz TS Sihra JM Delgado-García A Rodríguez-Moreno (2006) ArticleTitleKainate receptor-mediated inhibition of glutamate release involves protein kinase A in the mouse hippocampus J Neurophysiol 96 1829–1837 Occurrence Handle16807342 Occurrence Handle10.1152/jn.00280.2006 Occurrence Handle1:CAS:528:DC%2BD28XhtFSgtLnN
RE Nicholls X Zhang CP Bailey BR Conklin ER Kandel (2006) ArticleTitlemGluR2 acts through inhibitory Gα subunits to regulate transmission and long-term plasticity at hippocampal mossy fiber-CA3 synapses Proc Natl Acad Sci USA 103 6380–6385 Occurrence Handle16606834 Occurrence Handle10.1073/pnas.0601267103 Occurrence Handle1:CAS:528:DC%2BD28XktFamtrY%3D
RA Nicoll D Schmitz (2005) ArticleTitleSynaptic plasticity at hippocampal mossy fibre synapses Nat Rev Neurosci 6 863–876 Occurrence Handle16261180 Occurrence Handle10.1038/nrn1786 Occurrence Handle1:CAS:528:DC%2BD2MXhtFKls7nF
Y Park J Jo JTR Isaac K Cho (2006) ArticleTitleLong-term depression of kainate receptor-mediated synaptic transmission Neuron 49 95–106 Occurrence Handle16387642 Occurrence Handle10.1016/j.neuron.2005.11.035 Occurrence Handle1:CAS:528:DC%2BD28XntVGmtg%3D%3D
A Rodríguez-Moreno A Sistiaga J Lerma J Sánchez-Prieto (1998) ArticleTitleSwitch from facilitation to inhibition of excitatory synaptic transmission by group I mGluR desensitization Neuron 21 1477–1486 Occurrence Handle9883739 Occurrence Handle10.1016/S0896-6273(00)80665-0
A Rodríguez-Moreno JC López-García J Lerma (2000) ArticleTitleTwo populations of kainate receptors with separate signalling mechanisms in hippocampal interneurons Proc Natl Acad Sci USA 97 1293–1298 Occurrence Handle10655524 Occurrence Handle10.1073/pnas.97.3.1293
A Rodríguez-Moreno TS Sihra (2004) ArticleTitlePresynaptic kainate receptor facilitation of glutamate release involves protein kinase A in the rat hippocampus J Physiol 557 733–745 Occurrence Handle15107475 Occurrence Handle10.1113/jphysiol.2004.065029 Occurrence Handle1:CAS:528:DC%2BD2cXlslejtLs%3D
J Schmitz M Frerking RA Nicoll (2000) ArticleTitleSynaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses Neuron 27 327–338 Occurrence Handle10985352 Occurrence Handle10.1016/S0896-6273(00)00040-4 Occurrence Handle1:CAS:528:DC%2BD3cXmsVWmt7k%3D
D Schmitz J Mellor RA Nicoll (2001) ArticleTitlePresynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses Science 291 1972–1976 Occurrence Handle11239159 Occurrence Handle10.1126/science.1057105 Occurrence Handle1:CAS:528:DC%2BD3MXhvVSmtbw%3D
D Schmitz J Mellor J Breustedt RA Nicoll (2003) ArticleTitlePresynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation Nat Neurosci 6 1058–1063 Occurrence Handle12947409 Occurrence Handle10.1038/nn1116 Occurrence Handle1:CAS:528:DC%2BD3sXnsFamtLc%3D
T Tzounopoulos R Janz TC Sudhof RA Nicoll RC Malenka (1998) ArticleTitleA role for cAMP in long-term depression at hippocampal mossy fiber synapses Neuron 21 837–845 Occurrence Handle9808469 Occurrence Handle10.1016/S0896-6273(00)80599-1 Occurrence Handle1:CAS:528:DyaK1cXnt1Sgu7k%3D
MF Yeckel A Kapur D Johnston (1999) ArticleTitleMultiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism Nat Neurosci 2 625–633 Occurrence Handle10404192 Occurrence Handle10.1038/10180 Occurrence Handle1:CAS:528:DyaK1MXktFChuro%3D
M Yokoi K Kobayashi T Manabe T Takahashi I Sakaguchi G Katsuura R Shigemoto H Ohishi S Nomura K Nakamura K Nakao M Katsuki S Nakanishi (1996) ArticleTitleImpairment of hippocampal mossy fiber LTD in mice lacking mGluR2 Science 273 645–647 Occurrence Handle8662555 Occurrence Handle10.1126/science.273.5275.645 Occurrence Handle1:CAS:528:DyaK28Xks1yntLc%3D
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Negrete-Díaz, J., Sihra, T., Delgado-García, J. et al. Kainate receptor-mediated presynaptic inhibition converges with presynaptic inhibition mediated by Group II mGluRs and long-term depression at the hippocampal mossy fiber-CA3 synapse. J Neural Transm 114, 1425–1431 (2007). https://doi.org/10.1007/s00702-007-0750-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-007-0750-4