Switching off LTP: MGlu and NMDA receptor-dependent novelty exploration-induced depotentiation in the rat hippocampus

Cerebral Cortex

Volumn 23, Issue 4, 2013, Pages 932-939

  Qi, Yingjie ^a   Hu, Neng Wei ^a   Rowan, Michael J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

experience; learning; long term potentiation; synaptic plasticity

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; THETA RHYTHM;

ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; EXCITATORY AMINO ACID AGENTS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; WAKEFULNESS;

EID: 84875159782     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs086     Document Type: Article

References (46)

1. Abraham WC, Logan B, Greenwood JM, Dragunow M. 2002. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci. 22:9626-9634.
2. Barker GR, Bashir ZI, Brown MW, Warburton EC. 2006. A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory. Learn Mem. 13:178-186.
3. Bashir ZI, Collingridge GL. 1994. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp Brain Res. 100:437-443.
4. Clem RL, Huganir RL. 2010. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science. 330:1108-1112.
5. Collingridge GL, Peineau S, Howland JG, Wang YT. 2010. Long-term depression in the CNS. Nat Rev Neurosci. 11:459-473.
6. Diamond DM, Fleshner M, Rose GM. 1994. Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav Brain Res. 62:1-9.
7. Diaz-Mataix L, Debiec J, Ledoux JE, Doyere V. 2011. Sensory-specific associations stored in the lateral amygdala allow for selective alteration of fear memories. J Neurosci. 31:9538-9543.
8. Duffy S, Labrie V, Roder JC. 2008. D-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology. 33:1004-1018.
9. Fetterolf F, Foster KA. 2011. Regulation of long-term plasticity induction by the Channel and C-Terminal Domains of GluN2 subunits. Mol Neurobiol. 44:71-82.
10. Foy MR, Stanton ME, Levine S, Thompson RF. 1987. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol. 48:138-149.
11. Fujii S, Saito K, Miyakawa H, Ito K, Kato H. 1991. Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res. 555:112-122.
12. Ge Y, Dong Z, Bagot RC, Howland JG, Phillips AG, Wong TP, Wang YT. 2010. Hippocampal long-term depression is required for the consolidation of spatial memory. Proc Natl Acad Sci U S A. 107:16697-16702.
13. Gladding CM, Fitzjohn SM, Molnar E. 2009. Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol Rev. 61:395-412.
14. Green JD, Arduini AA. 1954. Hippocampal electrical activity in arousal. J Neurophysiol. 17:533-557.
15. Griffiths S, Scott H, Glover C, Bienemann A, Ghorbel MT, Uney J, Brown MW, Warburton EC, Bashir ZI. 2008. Expression of long-term depression underlies visual recognition memory. Neuron. 58:186-194.
16. Gruart A, Munoz MD, Delgado-Garcia JM. 2006. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci. 26:1077-1087.
17. Haley JE, Schaible E, Pavlidis P, Murdock A, Madison DV. 1996. Basal and apical synapses of CA1 pyramidal cells employ different LTP induction mechanisms. Learn Mem. 3:289-295.
18. Hirata R, Togashi H, Matsumoto M, Yamaguchi T, Izumi T, Yoshioka M. 2008. Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats. Brain Res. 1226:27-32.
19. Huang CC, Hsu KS. 2001. Progress in understanding the factors regulating reversibility of long-term potentiation. Rev Neurosci. 12:51-68.
20. Kemp A, Manahan-Vaughan D. 2004. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci U S A. 101:8192-8197.
21. Kim J, Lee S, Park K, Hong I, Song B, Son G, Park H, Kim WR, Park E, Choe HK, et al. 2007. Amygdala depotentiation and fear extinction. Proc Natl Acad Sci U S A. 104:20955-20960.
22. Kramar EA, Lynch G. 2003. Developmental and regional differences in the consolidation of long-term potentiation. Neuroscience. 118:387-398.
23. Kwon OB, Longart M, Vullhorst D, Hoffman DA, Buonanno A. 2005. Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J Neurosci. 25:9378-9383.
24. Leung LS, Shen B, Rajakumar N, Ma J. 2003. Cholinergic activity enhances hippocampal long-term potentiation in CA1 during walking in rats. J Neurosci. 23:9297-9304.
25. Li S, Cullen WK, Anwyl R, Rowan MJ. 2003. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat Neurosci. 6:526-531.
26. Luscher C, Huber KM. 2010. Group 1 mGluR-dependent synaptic longterm depression: mechanisms and implications for circuitry and disease. Neuron. 65:445-459.
27. Madronal N, Delgado-Garcia JM, Gruart A. 2007. Differential effects of long-term potentiation evoked at the CA3 CA1 synapse before, during, and after the acquisition of classical eyeblink conditioning in behaving mice. J Neurosci. 27:12139-12146.
28. Manahan-Vaughan D, Braunewell KH. 1999. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A. 96:8739-8744.
29. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature. 390:607-611.
30. Neves G, Cooke SF, Bliss TV. 2008. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci. 9:65-75.
31. Popkirov SG, Manahan-Vaughan D. 2011. Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor-dependent, learning-facilitated long-term depression in CA1 synapses. Cereb Cortex. 21:501-509.
32. Rogan MT, Staubli UV, LeDoux JE. 1997. Fear conditioning induces associative long-term potentiation in the amygdala. Nature. 390:604-607.
33. Rumpel S, LeDoux J, Zador A, Malinow R. 2005. Postsynaptic receptor trafficking underlying a form of associative learning. Science. 308:83-88.
34. Sajikumar S, Navakkode S, Frey JU. 2007. Identification of compartmentand process-specific molecules required for ''synaptic tagging'' during long-term potentiation and long-term depression in hippocampal CA1. J Neurosci. 27:5068-5080.
35. Sanderson TM, Cotel MC, O'Neill MJ, Tricklebank MD, Collingridge GL, Sher E. 2012. Alterations in hippocampal excitability, synaptic transmission and synaptic plasticity in a neurodevelopmental model of schizophrenia. Neuropharmacology. 62:1349-1358.
36. Staubli U, Lynch G. 1990. Stable depression of potentiated synaptic responses in the hippocampus with 1-5 Hz stimulation. Brain Res. 513:113-118.
37. Straube T, Korz V, Frey JU. 2003. Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci Lett. 344:5-8.
38. Valenzuela-Harrington M, Gruart A, Delgado-Garcia JM. 2007. Contribution of NMDA receptor NR2B subunit to synaptic plasticity during associative learning in behaving rats. Eur J Neurosci. 25:830-836.
39. Varty GB, Grilli M, Forlani A, Fredduzzi S, Grzelak ME, Guthrie DH, Hodgson RA, Lu SX, Nicolussi E, Pond AJ, et al. 2005. The antinociceptive and anxiolytic-like effects of the metabotropic glutamate receptor 5 (mGluR5) antagonists, MPEP and MTEP, and the mGluR1 antagonist, LY456236, in rodents: a comparison of efficacy and side-effect profiles. Psychopharmacology (Berl). 179:207-217.
40. Vitureira N, Letellier M, Goda Y. Forthcoming 2011. Homeostatic synaptic plasticity: from single synapses to neural circuits. Current Opin Neurobiol.
41. von Engelhardt J, Doganci B, Jensen V, Hvalby O, Gongrich C, Taylor A, Barkus C, Sanderson DJ, Rawlins JN, Seeburg PH, et al. 2008. Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron. 60:846-860.
42. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. 2006. Learning induces long-term potentiation in the hippocampus. Science. 313:1093-1097.
43. Xu J, Zhu Y, Contractor A, Heinemann SF. 2009. mGluR5 has a critical role in inhibitory learning. J Neurosci. 29:3676-3684.
44. Xu L, Anwyl R, Rowan MJ. 1998. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature. 394:891-894.
45. Yang CH, Huang CC, Hsu KS. 2006. Novelty exploration elicits a reversal of acute stress-induced modulation of hippocampal synaptic plasticity in the rat. J Physiol. 577:601-615.
46. Zhang M, Storm DR, Wang H. 2011. Bidirectional synaptic plasticity and spatial memory flexibility require Ca2+-stimulated adenylyl cyclases. J Neurosci. 31:10174-10183.