Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors

David Lodge, Patrick Tidball, Marion S Mercier, Sarah J Lucas, Lydia Hanna, Laura Ceolin, Minos Kritikos, Stephen M Fitzjohn, John L Sherwood, Neil Bannister, Arturas Volianskis, David E Jane, Zuner A Bortolotto, Graham L Collingridge

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Metabotropic glutamate (mGlu) receptors are implicated in many neurological and psychiatric diseases and are the targets of therapeutic agents currently in clinical development. Their activation has diverse effects in the central nervous system (CNS) that includes an involvement in synaptic plasticity. We previously reported that the brief exposure of hippocampal slices to dihydroxyphenylglycine (DHPG) can result in a long-term depression (LTD) of excitatory synaptic transmission. Surprisingly, this LTD could be fully reversed by mGlu receptor antagonists in a manner that was itself fully reversible upon washout of the antagonist. Here, 15 years after the discovery of DHPG-LTD and its reversible reversibility, we summarise these initial findings. We then present new data on DHPG-LTD, which demonstrates that evoked epileptiform activity triggered by activation of group I mGlu receptors can also be reversibly reversed by mGlu receptor antagonists. Furthermore, we show that the phenomenon of reversible reversibility is not specific to group I mGlu receptors. We report that activation of group II mGlu receptors in the temporo-ammonic pathway (TAP) and mossy fibre pathway within the hippocampus and in the cortical input to neurons of the lateral amygdala induces an LTD that is reversed by LY341495, a group II mGlu receptor antagonist. We also show that activation of group III mGlu8 receptors induces an LTD at lateral perforant path inputs to the dentate gyrus and that this LTD is reversed by MDCPG, an mGlu8 receptor antagonist. In conclusion, we have shown that activation of representative members of each of the three groups of mGlu receptors can induce forms of LTD than can be reversed by antagonists, and that in each case washout of the antagonist is associated with the re-establishment of the LTD. This article is part of the Special Issue entitled 'Glutamate Receptor-Dependent Synaptic Plasticity'.

Original languageEnglish
Pages (from-to)135-146
Number of pages12
JournalNeuropharmacology
Volume74
Early online date26 Mar 2013
DOIs
Publication statusPublished - Nov 2013

Fingerprint

Metabotropic Glutamate Receptors
Excitatory Amino Acid Antagonists
Neuronal Plasticity
LY 341495
Perforant Pathway
Dentate Gyrus
Glutamate Receptors
Amygdala
Synaptic Transmission
Psychiatry
Hippocampus
Central Nervous System
Neurons

Keywords

  • Amino Acids
  • Animals
  • Brain
  • Excitatory Amino Acid Antagonists
  • Glycine
  • Long-Term Synaptic Depression
  • Mice
  • Neural Pathways
  • Rats
  • Receptors, Metabotropic Glutamate
  • Xanthenes

Cite this

Lodge, D., Tidball, P., Mercier, M. S., Lucas, S. J., Hanna, L., Ceolin, L., ... Collingridge, G. L. (2013). Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors. Neuropharmacology, 74, 135-146. https://doi.org/10.1016/j.neuropharm.2013.03.011

Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors. / Lodge, David; Tidball, Patrick; Mercier, Marion S; Lucas, Sarah J; Hanna, Lydia; Ceolin, Laura; Kritikos, Minos; Fitzjohn, Stephen M; Sherwood, John L; Bannister, Neil; Volianskis, Arturas; Jane, David E; Bortolotto, Zuner A; Collingridge, Graham L.

In: Neuropharmacology, Vol. 74, 11.2013, p. 135-146.

Research output: Contribution to journalArticle

Lodge, D, Tidball, P, Mercier, MS, Lucas, SJ, Hanna, L, Ceolin, L, Kritikos, M, Fitzjohn, SM, Sherwood, JL, Bannister, N, Volianskis, A, Jane, DE, Bortolotto, ZA & Collingridge, GL 2013, 'Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors', Neuropharmacology, vol. 74, pp. 135-146. https://doi.org/10.1016/j.neuropharm.2013.03.011
Lodge, David ; Tidball, Patrick ; Mercier, Marion S ; Lucas, Sarah J ; Hanna, Lydia ; Ceolin, Laura ; Kritikos, Minos ; Fitzjohn, Stephen M ; Sherwood, John L ; Bannister, Neil ; Volianskis, Arturas ; Jane, David E ; Bortolotto, Zuner A ; Collingridge, Graham L. / Antagonists reversibly reverse chemical LTD induced by group I, group II and group III metabotropic glutamate receptors. In: Neuropharmacology. 2013 ; Vol. 74. pp. 135-146.
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AU - Lodge, David

AU - Tidball, Patrick

AU - Mercier, Marion S

AU - Lucas, Sarah J

AU - Hanna, Lydia

AU - Ceolin, Laura

AU - Kritikos, Minos

AU - Fitzjohn, Stephen M

AU - Sherwood, John L

AU - Bannister, Neil

AU - Volianskis, Arturas

AU - Jane, David E

AU - Bortolotto, Zuner A

AU - Collingridge, Graham L

N1 - Copyright © 2013 Elsevier Ltd. All rights reserved.

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N2 - Metabotropic glutamate (mGlu) receptors are implicated in many neurological and psychiatric diseases and are the targets of therapeutic agents currently in clinical development. Their activation has diverse effects in the central nervous system (CNS) that includes an involvement in synaptic plasticity. We previously reported that the brief exposure of hippocampal slices to dihydroxyphenylglycine (DHPG) can result in a long-term depression (LTD) of excitatory synaptic transmission. Surprisingly, this LTD could be fully reversed by mGlu receptor antagonists in a manner that was itself fully reversible upon washout of the antagonist. Here, 15 years after the discovery of DHPG-LTD and its reversible reversibility, we summarise these initial findings. We then present new data on DHPG-LTD, which demonstrates that evoked epileptiform activity triggered by activation of group I mGlu receptors can also be reversibly reversed by mGlu receptor antagonists. Furthermore, we show that the phenomenon of reversible reversibility is not specific to group I mGlu receptors. We report that activation of group II mGlu receptors in the temporo-ammonic pathway (TAP) and mossy fibre pathway within the hippocampus and in the cortical input to neurons of the lateral amygdala induces an LTD that is reversed by LY341495, a group II mGlu receptor antagonist. We also show that activation of group III mGlu8 receptors induces an LTD at lateral perforant path inputs to the dentate gyrus and that this LTD is reversed by MDCPG, an mGlu8 receptor antagonist. In conclusion, we have shown that activation of representative members of each of the three groups of mGlu receptors can induce forms of LTD than can be reversed by antagonists, and that in each case washout of the antagonist is associated with the re-establishment of the LTD. This article is part of the Special Issue entitled 'Glutamate Receptor-Dependent Synaptic Plasticity'.

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