Metabotropic glutamate receptor 1 (mGluR1) and 5 (mGluR5) regulate late phases of LTP and LTD in the hippocampal CA1 region in vitro

Abstract

The group I metabotropic glutamate receptors, mGluR1 and mGluR5, exhibit differences in their regulation of synaptic plasticity, suggesting that these receptors may subserve separate functional roles in information storage. In addition, although effects in vivo are consistently described, conflicting reports of the involvement of mGluRs in hippocampal synaptic plasticity in vitro exist. We therefore addressed the involvement of mGluR1 and mGluR5 in long‐term potentiation (LTP) and long‐term depression (LTD) in the hippocampal CA1 region of adult male rats in vitro . The mGluR1 antagonist (S)‐(+)‐α‐amino‐4‐carboxy‐2‐methylbenzene‐acetic acid (LY367385) impaired both induction and late phases of both LTP and LTD, when applied before high‐frequency tetanization (HFT; 100 Hz) or low‐frequency stimulation (LFS; 1 Hz), respectively. Application after either HFT or LFS had no effect. The mGluR5 antagonist 2‐methyl‐6‐(phenylethynyl)pyridine (MPEP), when given before HFT, inhibited both the induction and late phases of LTP. When given after HFT, late LTP was inhibited. MPEP, given prior to LFS, impaired LTD induction, although stable LTD was still expressed. Application after LFS significantly impaired late phases of LTD. Activation of protein synthesis may comprise a key mechanism underlying the group I mGluR contribution to synaptic plasticity. The mGluR5 agonist (R,S)‐2‐chloro‐5‐hydroxyphenylglycine (CHPG) converted short‐term depression into LTD. Effects were prevented by application of the protein synthesis inhibitor anisomycin, suggesting that protein synthesis is triggered by group I mGluR activation to enable persistency of synaptic plasticity. Taken together, these data support the notion that both mGluR1 and mGluR5 are critically involved in bidirectional synaptic plasticity in the CA1 region and may enable functional differences in information encoding through LTP and LTD.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 56

1. 1.

   Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, Tonegawa S. Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell. 1994;79:365-375.

   Not in our library10.1016/0092-8674(94)90204-6

2. 2.

   Attucci S, Carla V, Mannaioni G, Moroni F. Activation of type 5 metabotropic glutamate receptors enhances NMDA responses in mice cortical wedges. Br. J. Pharmacol. 2001;132:799-806.

   Not in our library10.1038/sj.bjp.0703904

3. 3.

   Balschun D, Manahan-Vaughan D, Wagner T, Behnisch T, Reymann KG, Wetzel W. A specific role for group I mGluRs in hippocampal LTP and hippocampus- dependent spatial learning. Learn. Mem. 1999;6:138-152.

   Not in our library

4. 4.

   Balschun D, Wetzel W. Inhibition of mGluR5 blocks hippocampal LTP in vivo and spatial learning in rats. Pharmacol. Biochem. Behav. 2002;73:375-380.

   Not in our library10.1016/s0091-3057(02)00847-x

5. 5.

   Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL. A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature. 1999;368:740-743.

   Not in our library10.1038/368740a0

6. 6.

   Carlier E, Sourdet V, Boudkkazi S, Deglise P, Ankri N, Fronzaroli-Molinieres L, Debanne D. Metabotropic glutamate receptor subtype 1 regulates sodium currents in rat neocortical pyramidal neurons. J. Physiol. (Lond.). 2006;577:141-154.

   Not in our library10.1113/jphysiol.2006.118026

7. 7.

   Chinestra P, Aniksztejn L, Diabira D, Ben-Ari Y. (RS)-alpha-methyl-4-carboxyphenylglycine neither prevents induction of LTP nor antagonizes metabotropic glutamate receptors in CA1 hippocampal neurons. J. Neurophysiol. 1993;70:2684-2689.

   Not in our library10.1152/jn.1993.70.6.2684

8. 8.

   Clark BP, Baker SR, Goldsworthy J, Harris JR, Kingston AE. (+)-2-Methyl-4-carboxyphenylglycine (LY367385) selectively antagonises metabotropic glutamate mGlu1 receptors. Biorg. Med. Chem. Lett. 1997;7:2777-2780.

   Not in our library

9. 9.

   Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature. 1994;372:237-243.

   Not in our library10.1038/372237a0

10. 10.

    Doherty AJ, Palmer MJ, Bortolotto ZA, Hargreaves A, Kingston AE, Ornstein PL, Schoepp DD, Lodge D, Collingridge GL. A novel, competitive mGlu (5) receptor antagonist (LY344545) blocks DHPG-induced potentiation of NMDA responses but not the induction of LTP in rat hippocampal slices. Br. J. Pharmacol. 2000;131:239-244.

    Not in our library10.1038/sj.bjp.0703574

11. 11.

    Dunwiddie T, Madison D, Lynch G. Synaptic transmission is required for initiation of long-term potentiation. Brain Res. 1978;150:413-417.

    Not in our library10.1016/0006-8993(78)90293-7

12. 12.

    Etkin A, Alarcon JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, Kandel ER. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron. 2006;50:127-143.

    Not in our library10.1016/j.neuron.2006.03.013

13. 13.

    Fitzjohn SM, Kingston AE, Lodge D, Collingridge GL. DHPG-induced LTD in area CA1 of juvenile rat hippocampus; characterisation and sensitivity to novel mGlu receptor antagonists. Neuropharmacology. 1999;38:1577-1583.

    Not in our library10.1016/s0028-3908(99)00123-9

14. 14.

    Fitzjohn SM, Palmer MJ, May JER, Neeson A, Morris SAC, Collingridge GL. A characterisation of long-term depression induced by metabotropic glutamate receptor activation in the rat hippocampus in vitro. J. Physiol. (Lond.). 2001;537:421-430.

    Not in our library10.1111/j.1469-7793.2001.00421.x

15. 15.

    Francesconi W, Cammalleri M, Sanna PP. The metabotropic glutamate receptor 5 is necessary for late-phase long-term potentiation in the hippocampal CA1 region. Brain Res. 2004;1022:12-18.

    Not in our library10.1016/j.brainres.2004.06.060

16. 16.

    Frey U, Krug M, Reymann KG, Matthies H. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res. 1988;452:57-65.

    Not in our library10.1016/0006-8993(88)90008-x

17. 17.

    Gasparini F, Lingenhohl K, Stoehr N, Flor PJ, Heinrich M, Vranesic I, Biollaz M, Allgeier H, Heckendorn R, Urwyler S, Varney MA, Johnson EC, Hess SD, Rao SP, Sacaan AI, Santori EM, Veliceleb, i G, Kuhn R. 2-Methyl-6-(phenylethynyl) -pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology. 1999;38:1493-1503.

    Not in our library10.1016/s0028-3908(99)00082-9

18. 18.

    Harney SC, Rowan M, Anwyl R. Long-term depression of NMDA receptor-mediated synaptic transmission is dependent on activation of metabotropic glutamate receptors and is altered to long-term potentiation by low intracellular calcium buffering. J. Neurosci. 2006;26:1128-1132.

    Not in our library10.1523/jneurosci.2753-05.2006

19. 19.

    Hou L, Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor- dependent long-term depression. J. Neurosci. 2004;24:6352-6361.

    Not in our library10.1523/jneurosci.0995-04.2004

20. 20.

    Huber KM, Roder JC, Bear MF. Chemical induction of mGluR5- and protein synthesis-dependent long-term depression in hippocampal area CA1. J. Neurophysiol. 2001;86:321-325.

    Not in our library10.1152/jn.2001.86.1.321

21. 21.

    Ireland DR, Abraham WC. Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J. Neurophysiol. 2002;88:107-116.

    Not in our library10.1152/jn.2002.88.1.107

22. 22.

    Ireland DR, Guevremont D, Williams JM, Abraham WC. Metabotropic glutamate receptor-mediated depression of the slow afterhyperpolarization is gated by tyrosine phosphatases in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2004;92:2811-2819.

    Not in our library10.1152/jn.01236.2003

23. 23.

    Jia Z, Lu Y, Henderson J, Taverna F, Romano C, Abramow-Newerly W, Wojtowicz JM, Roder J. Selective abolition of the NMDA component of long-term potentiation in mice lacking mGluR5. Learn. Mem. 1998;5:331-343.

    Not in our library

24. 24.

    Joly C, Gomeza J, Brabet I, Curry K, Bockaert J, Pin JP. Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1. J. Neurosci. 1995;15:3970-3981.

    Not in our library10.1523/jneurosci.15-05-03970.1995

25. 25.

    Kemp A, Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl Acad. Sci. USA. 2004;101:8192-8197.

    Not in our library10.1073/pnas.0402650101

26. 26.

    Kemp A, Manahan-Vaughan D. The 5-hydroxytryptamine4 receptor exhibits frequency-dependent properties in synaptic plasticity and behavioural metaplasticity in the hippocampal CA1 region in vivo. Cereb. Cortex. 2005;15:1037-1043.

    Not in our library10.1093/cercor/bhh204

27. 27.

    Kemp A, Manahan-Vaughan D. Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci. 2007;30:111-118.

    Not in our library10.1016/j.tins.2007.01.002

28. 28.

    Lan JY, Skeberdis VA, Jover T, Zheng X, Bennett MV, Zukin RS. Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J. Neurosci. 2001;21:6058-6068.

    Not in our library10.1523/jneurosci.21-16-06058.2001

29. 29.

    Li B, Chen N, Luo T, Otsu Y, Murphy TH, Raymond LA. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nat. Neurosci. 2002;5:833-834.

    Not in our library10.1038/nn912

30. 30.

    Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 1997;17:5196-5205.

    Not in our library10.1523/jneurosci.17-13-05196.1997

31. 31.

    Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 1996;8:1488-1500.

    Not in our library10.1111/j.1460-9568.1996.tb01611.x

32. 32.

    Manahan-Vaughan D. Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J. Neurosci. 1997;17:3303-3311.

    Not in our library10.1523/jneurosci.17-09-03303.1997

33. 33.

    Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl Acad. Sci. USA. 1999;96:8739-8744.

    Not in our library10.1073/pnas.96.15.8739

34. 34.

    Manahan-Vaughan D, Braunewell KH. The metabotropic glutamate receptor, mGluR5, is a key determinant of good and bad spatial learning performance and hippocampal synaptic plasticity. Cereb. Cortex. 2005;15:1703-1713.

    Not in our library10.1093/cercor/bhi047

35. 35.

    Manahan-Vaughan D, Braunewell KH, Reymann KG. Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats. Neuroscience. 1998;86:709-721.

    Not in our library10.1016/s0306-4522(98)00111-0

36. 36.

    Manahan-Vaughan D, Herrero I, Reymann KG, Sanchez-Prieto J. Presynaptic group 1 metabotropic glutamate receptors may contribute to the expression of long-term potentiation in the hippocampal CA1 region. Neuroscience. 1999;94:71-82.

    Not in our library10.1016/s0306-4522(99)00266-3

37. 37.

    Manahan-Vaughan D, Ngomba RT, Storto M, Kulla A, Catania MV, Chiechio S, Rampello L, Passarelli F, Capece A, Reymann KG, Nicoletti F. An increased expression of the mGlu5 receptor protein following LTP induction at the perforant path-dentate gyrus synapse in freely moving rats. Neuropharmacology. 2003;44:17-25.

    Not in our library10.1016/s0028-3908(02)00342-8

38. 38.

    Manahan-Vaughan D, Reymann KG. Metabotropic glutamate receptor subtype agonists facilitate long-term potentiation within a distinct time window in the dentate gyrus in vivo. Neuroscience. 1996;74:723-731.

    Not in our library10.1016/0306-4522(96)00162-5

39. 39.

    Manahan-Vaughan D, Reymann KG. Metabotropic glutamate receptor subtype agonists facilitate long-term potentiation within a distinct time window in the dentate gyrus in vivo. Neuroscience. 1996;74:723-731.

    Not in our library10.1016/0306-4522(96)00162-5

40. 40.

    Mannaioni G, Marino MJ, Valenti O, Traynelis SF, Conn PJ. Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J. Neurosci. 2001;21:5925-5934.

    Not in our library10.1523/jneurosci.21-16-05925.2001

41. 41.

    Manzoni OJ, Weisskopf MG, Nicoll RA. MCPG antagonizes metabotropic glutamate receptors but not long-term potentiation in the hippocampus. Eur. J. Neurosci. 1994;6:1050-1054.

    Not in our library10.1111/j.1460-9568.1994.tb00599.x

42. 42.

    Miura M, Watanabe M, Offermanns S, Simon MI, Kano M. Group I metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J. Neurosci. 2002;22:8379-8390.

    Not in our library10.1523/jneurosci.22-19-08379.2002

43. 43.

    Naie K, Manahan-Vaughan D. Regulation by metabotropic glutamate receptor 5 of LTP in the dentate gyrus of freely moving rats: relevance for learning and memory formation. Cereb. Cortex. 2004;14:189-198.

    Not in our library10.1093/cercor/bhg118

44. 44.

    Naie K, Manahan-Vaughan D. Pharmacological antagonism of metabotropic glutamate receptor 1 regulates long-term potentiation and spatial reference memory in the dentate gyrus of freely moving rats via N-methyl-D-aspartate and metabotropic glutamate receptor-dependent mechanisms. Eur. J. Neurosci. 2005;21:411-421.

    Not in our library10.1111/j.1460-9568.2005.03864.x

45. 45.

    Naie K, Tsanov M, Manahan-Vaughan D. Group I metabotropic glutamate receptors enable two distinct forms of long-term depression in the rat dentate gyrus in vivo. Eur. J. Neurosci. 2007;25:3264-3275.

    Not in our library10.1111/j.1460-9568.2007.05583.x

46. 46.

    Rae MG, Irving AJ. Both mGluR1 and mGluR5 mediate Ca2+ release and inward currents in hippocampal CA1 pyramidal neurons. Neuropharmacology. 2004;46:1057-1069.

    Not in our library10.1016/j.neuropharm.2004.02.002

47. 47.

    Raymond CR, Thompson VL, Tate WP, Abraham W, C. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J. Neurosci. 2000;20:969-976.

    Not in our library10.1523/jneurosci.20-03-00969.2000

48. 48.

    Roche KW, Standley S, McCallum J, Dune Ly C, Ehlers MD, Wenthold RJ. determinants of NMDA receptor internalization. Nat. Neurosci. 2001;4:794-802.

    Not in our library10.1038/90498

49. 49.

    Selig DK, Lee HK, Bear MF, Malenka RC. Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J. Neurophysiol. 1995;74:1075-1082.

    Not in our library10.1152/jn.1995.74.3.1075

50. 50.

    Skeberdis VA, Lan J, Opitz T, Zheng X, Bennett MV, Zukin RS. mGluR1-mediated potentiation of NMDA receptors involves a rise in intracellular calcium and activation of protein kinase C. Neuropharmacology. 2001;40:856-865.

    Not in our library10.1016/s0028-3908(01)00005-3

51. 51.

    Thomas MJ, O'Dell TJ. The molecular switch hypothesis fails to explain the inconsistent effects of the metabotropic glutamate receptor antagonist MCPG on long-term potentiation. Brain Res. 1995;695:45-52.

    Not in our library10.1016/0006-8993(95)00757-h

52. 52.

    Topolnik L, Azzi M, Morin F, Kougioumoutzakis A, Lacaille JC. mGluR1/5 subtype-specific calcium signalling and induction of long-term potentiation in rat hippocampal oriens/alveus interneurones. J. Physiol. (Lond.). 2006;575:115-131.

    Not in our library10.1113/jphysiol.2006.112896

53. 53.

    Uzakov S, Frey JU, Korz V. Reinforcement of rat hippocampal LTP by holeboard training. Learn. Mem. 2005;12:165-171.

    Not in our library10.1101/lm.89305

54. 54.

    Volk LJ, Daly CA, Huber KM. Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression. J. Neurophysiol. 2006;95:2427-2438.

    Not in our library10.1152/jn.00383.2005

55. 55.

    Wilsch VW, Behnisch T, Jäger T, Reymann KG, Balschun D. When are class I metabotropic glutamate receptors necessary for long-term potentiation? J. Neurosci. 1998;18:6071-6080.

    Not in our library10.1523/jneurosci.18-16-06071.1998

56. 56.

    Wu J, Rush A, Rowan MJ, Anwyl R. NMDA receptor- and metabotropic glutamate receptor-dependent synaptic plasticity induced by high frequency stimulation in the rat dentate gyrus in vitro. J. Physiol. (Lond.). 2001;533:745-755.

    Not in our library10.1111/j.1469-7793.2001.t01-1-00745.x

Cited by papers we hold 2

• Separate ionotropic and metabotropic glutamate receptor functions in depotentiation versus LTP: A distinct role for group1 mGluR subtypes and NMDARs · 2016
  Not checked
• Successful cognitive aging in rats: a role for mGluR5 glutamate receptors, homer 1 proteins and downstream signaling pathways. · 2012
  Not checked

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.