Skip to main content
SpringerLink
Log in

Developmental alterations of DHPG-induced long-term depression of corticostriatal synaptic transmission: switch from NMDA receptor-dependent towards CB1 receptor-dependent plasticity

  • Neuroscience
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

An Erratum to this article was published on 09 September 2009

Abstract

In animal models of early Parkinson’s disease (PD), motor deficits are accompanied by excessive striatal glutamate release. Blockade of group I metabotropic glutamate receptors (mGluRs), endocannabinoid degradation and nitric oxide (NO) synthesis combats PD symptoms. Activation of group I mGluRs with the specific agonist 3,5-dihydroxyphenylglycine (DHPG) induces long-term depression of corticostriatal transmission (LTDDHPG) in the adult mouse striatum requiring NO synthesis downstream to cannabinoid CB1 receptor (CB1R) activation suggesting a dual role for LTDDHPG: neuroprotective by down-regulation of glutamatergic transmission and, under certain circumstances, neurotoxic by release of NO. We report now that LTDDHPG undergoes a developmental switch from N-methyl-D-aspartate (NMDA)-receptor-dependent/CB1R-independent to NMDA receptor-independent/CB1R-dependent plasticity with NO playing an essential role for LTDDHPG at all developmental stages. The gain in function of CB1R is explained by their developmental up-regulation evaluated with real-time reverse transcription-polymerase chain reaction. These findings are relevant for the pathophysiology and therapy of PD as they link the activation of group I mGluRs, endocannabinoid release, and striatal NO production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ade KK, Lovinger DM (2007) Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci 27:2403–2409

    Article  PubMed  CAS  Google Scholar 

  2. Azad SC, Marsicano G, Eberlein I, Putzke J, Zieglgansberger W, Spanagel R, Lutz B (2001) Differential role of the nitric oxide pathway on delta(9)-THC-induced central nervous system effects in the mouse. Eur J NeuroSci 13:561–568

    Article  PubMed  CAS  Google Scholar 

  3. Bellone C, Luscher C, Mameli M (2008) Mechanisms of synaptic depression triggered by metabotropic glutamate receptors. Cell Mol Life Sci 65:2913–2923

    Article  PubMed  CAS  Google Scholar 

  4. Bloomfield C, O’Donnell P, French SJ, Totterdell S (2007) Cholinergic neurons of the adult rat striatum are immunoreactive for glutamatergic N-methyl-d-aspartate 2D but not N-methyl-d-aspartate 2C receptor subunits. Neuroscience 150:639–646

    Article  PubMed  CAS  Google Scholar 

  5. Bredt DS (2003) Nitric oxide signaling in brain: potentiating the gain with YC-1. Mol Pharmacol 63:1206–1208

    Article  PubMed  CAS  Google Scholar 

  6. Calabresi P, Galletti F, Saggese E, Ghiglieri V, Picconi B (2007) Neuronal networks and synaptic plasticity in Parkinson’s disease: beyond motor deficits. Parkinsonism Relat Disord 13(Suppl 3):S259–S262

    Article  PubMed  Google Scholar 

  7. Calabresi P, Gubellini P, Centonze D, Sancesario G, Morello M, Giorgi M, Pisani A, Bernardi G (1999) A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J Neurosci 19:2489–2499

    PubMed  CAS  Google Scholar 

  8. Catania MV, Landwehrmeyer GB, Testa CM, Standaert DG, Penney JB Jr, Young AB (1994) Metabotropic glutamate receptors are differentially regulated during development. Neuroscience 61:481–495

    Article  PubMed  CAS  Google Scholar 

  9. Centonze D, Gubellini P, Pisani A, Bernardi G, Calabresi P (2003) Dopamine, acetylcholine and nitric oxide systems interact to induce corticostriatal synaptic plasticity. Rev Neurosci 14:207–216

    PubMed  CAS  Google Scholar 

  10. Chalimoniuk M, Langfort J, Lukacova N, Marsala J (2004) Upregulation of guanylyl cyclase expression and activity in striatum of MPTP-induced parkinsonism in mice. Biochem Biophys Res Commun 324:118–126

    Article  PubMed  CAS  Google Scholar 

  11. Choi S, Lovinger DM (1997) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci U S A 94:2665–2670

    Article  PubMed  CAS  Google Scholar 

  12. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205–237

    Article  PubMed  CAS  Google Scholar 

  13. Coutinho V, Knopfel T (2002) Metabotropic glutamate receptors: electrical and chemical signaling properties. Neuroscientist 8:551–561

    Article  PubMed  CAS  Google Scholar 

  14. Cull-Candy SG, Leszkiewicz DN (2004) Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004:re16

    Article  PubMed  Google Scholar 

  15. D’Ascenzo M, Fellin T, Terunuma M, Revilla-Sanchez R, Meaney DF, Auberson YP, Moss SJ, Haydon PG (2007) mGluR5 stimulates gliotransmission in the nucleus accumbens. Proc Natl Acad Sci U S A 104:1995–2000

    Article  PubMed  CAS  Google Scholar 

  16. Dang MT, Yokoi F, Yin HH, Lovinger DM, Wang Y, Li Y (2006) Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum. Proc Natl Acad Sci U S A 103:15254–15259

    Article  PubMed  CAS  Google Scholar 

  17. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9:251–259

    Article  PubMed  CAS  Google Scholar 

  18. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, Piomelli D (1994) Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372:686–691

    Article  PubMed  Google Scholar 

  19. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7–61

    PubMed  CAS  Google Scholar 

  20. Domenici MR, Pepponi R, Martire A, Tebano MT, Potenza RL, Popoli P (2004) Permissive role of adenosine A2A receptors on metabotropic glutamate receptor 5 (mGluR5)-mediated effects in the striatum. J Neurochem 90:1276–1279

    Article  PubMed  CAS  Google Scholar 

  21. Dunah AW, Standaert DG (2003) Subcellular segregation of distinct heteromeric NMDA glutamate receptors in the striatum. J Neurochem 85:935–943

    PubMed  CAS  Google Scholar 

  22. Fellin T, D’Ascenzo M, Haydon PG (2007) Astrocytes control neuronal excitability in the nucleus accumbens. Scientific WorldJournal 7:89–97

    Google Scholar 

  23. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446–451

    PubMed  CAS  Google Scholar 

  24. Gubellini P, Pisani A, Centonze D, Bernardi G, Calabresi P (2004) Metabotropic glutamate receptors and striatal synaptic plasticity: implications for neurological diseases. Prog Neurobiol 74:271–300

    Article  PubMed  CAS  Google Scholar 

  25. Hermans E, Challiss RA (2001) Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors: prototypic family C G-protein-coupled receptors. Biochem J 359:465–484

    Article  PubMed  CAS  Google Scholar 

  26. Holscher C, Gigg J, O’Mara SM (1999) Metabotropic glutamate receptor activation and blockade: their role in long-term potentiation, learning and neurotoxicity. Neurosci Biobehav Rev 23:399–410

    Article  PubMed  CAS  Google Scholar 

  27. Hurst RS, Cepeda C, Shumate LW, Levine MS (2001) Delayed postnatal development of NMDA receptor function in medium-sized neurons of the rat striatum. Dev Neurosci 23:122–134

    Article  PubMed  CAS  Google Scholar 

  28. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M, Mackie K, Piomelli D (2005) Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 68:1196–1202

    Article  PubMed  CAS  Google Scholar 

  29. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380

    Article  PubMed  CAS  Google Scholar 

  30. Kasanetz F, Manzoni OJ (2009) Maturation of excitatory synaptic transmission of the rat nucleus accumbens from juvenile to adult. J Neurophysiol 101:2516–2527

    Article  PubMed  CAS  Google Scholar 

  31. Kerner JA, Standaert DG, Penney JB Jr, Young AB, Landwehrmeyer GB (1997) Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Brain Res Mol Brain Res 48:259–269

    Article  PubMed  CAS  Google Scholar 

  32. Kosinski CM, Standaert DG, Counihan TJ, Scherzer CR, Kerner JA, Daggett LP, Velicelebi G, Penney JB, Young AB, Landwehrmeyer GB (1998) Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: striatum and globus pallidus. J Comp Neurol 390:63–74

    Article  PubMed  CAS  Google Scholar 

  33. Kreitzer AC, Malenka RC (2005) Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25:10537–10545

    Article  PubMed  CAS  Google Scholar 

  34. Kreitzer AC, Malenka RC (2007) Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature 445:643–647

    Article  PubMed  CAS  Google Scholar 

  35. Lau WK, Lui PW, Wong CK, Chan YS, Yung KK (2003) Differential expression of N-methyl-D-aspartate receptor subunit messenger ribonucleic acids and immunoreactivity in the rat neostriatum during postnatal development. Neurochem Int 43:47–65

    Article  PubMed  CAS  Google Scholar 

  36. Logan SM, Partridge JG, Matta JA, Buonanno A, Vicini S (2007) Long-lasting NMDA receptor-mediated EPSCs in mouse striatal medium spiny neurons. J Neurophysiol 98:2693–2704

    Article  PubMed  CAS  Google Scholar 

  37. Maccarrone M, Fiori A, Bari M, Granata F, Gasperi V, De Stefano ME, Finazzi-Agro A, Strom R (2006) Regulation by cannabinoid receptors of anandamide transport across the blood-brain barrier and through other endothelial cells. Thromb Haemost 95:117–127

    PubMed  CAS  Google Scholar 

  38. Maccarrone M, Rossi S, Bari M, De Chiara V, Fezza F, Musella A, Gasperi V, Prosperetti C, Bernardi G, Finazzi-Agro A, Cravatt BF, Centonze D (2008) Anandamide inhibits metabolism and physiological actions of 2-arachidonoylglycerol in the striatum. Nat Neurosci 11:152–159

    Article  PubMed  CAS  Google Scholar 

  39. Mao L, Wang JQ (2002) Interactions between ionotropic and metabotropic glutamate receptors regulate cAMP response element-binding protein phosphorylation in cultured striatal neurons. Neuroscience 115:395–402

    Article  PubMed  CAS  Google Scholar 

  40. Mao L, Wang JQ (2003) Group I metabotropic glutamate receptor-mediated calcium signalling and immediate early gene expression in cultured rat striatal neurons. Eur J NeuroSci 17:741–750

    Article  PubMed  Google Scholar 

  41. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540

    Article  PubMed  CAS  Google Scholar 

  42. Ohashi S, Mori A, Kurihara N, Mitsumoto Y, Nakai M (2006) Age-related severity of dopaminergic neurodegeneration to MPTP neurotoxicity causes motor dysfunction in C57BL/6 mice. Neurosci Lett 401:183–187

    Article  PubMed  CAS  Google Scholar 

  43. Orlando LR, Alsdorf SA, Penney JB Jr, Young AB (2001) The role of group I and group II metabotropic glutamate receptors in modulation of striatal NMDA and quinolinic acid toxicity. Exp Neurol 167:196–204

    Article  PubMed  CAS  Google Scholar 

  44. Partridge JG, Tang KC, Lovinger DM (2000) Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84:1422–1429

    PubMed  CAS  Google Scholar 

  45. Petralia RS, Sans N, Wang YX, Wenthold RJ (2005) Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29:436–452

    Article  PubMed  CAS  Google Scholar 

  46. Pisani A, Bernardi G, Bonsi P, Centonze D, Giacomini P, Calabresi P (2000) Cell-type specificity of mGluR activation in striatal neuronal subtypes. Amino Acids 19:119–129

    Article  PubMed  CAS  Google Scholar 

  47. Pisani A, Bernardi G, Ding J, Surmeier DJ (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci 30:545–553

    Article  PubMed  CAS  Google Scholar 

  48. Pisani A, Calabresi P, Centonze D, Bernardi G (1997) Enhancement of NMDA responses by group I metabotropic glutamate receptor activation in striatal neurones. Br J Pharmacol 120:1007–1014

    Article  PubMed  CAS  Google Scholar 

  49. Pisani A, Gubellini P, Bonsi P, Conquet F, Picconi B, Centonze D, Bernardi G, Calabresi P (2001) Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-D-aspartate responses in medium spiny striatal neurons. Neuroscience 106:579–587

    Article  PubMed  CAS  Google Scholar 

  50. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci U S A 99:8384–8388

    Article  PubMed  CAS  Google Scholar 

  51. Ronesi J, Gerdeman GL, Lovinger DM (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J Neurosci 24:1673–1679

    Article  PubMed  CAS  Google Scholar 

  52. Schulz D, Sergeeva OA, Ianovskii E, Luhmann HJ, Haas HL, Huston JP (2004) Behavioural parameters in aged rats are related to LTP and gene expression of ChAT and NMDA-NR2 subunits in the striatum. Eur J NeuroSci 19:1373–1383

    Article  PubMed  CAS  Google Scholar 

  53. Senkowska A, Ossowska K (2003) Role of metabotropic glutamate receptors in animal models of Parkinson’s disease. Pol J Pharmacol 55:935–950

    PubMed  CAS  Google Scholar 

  54. Sergeeva OA, Chepkova AN, Doreulee N, Eriksson KS, Poelchen W, Monnighoff I, Heller-Stilb B, Warskulat U, Haussinger D, Haas HL (2003) Taurine-induced long-lasting enhancement of synaptic transmission in mice: role of transporters. J Physiol 550:911–919

    Article  PubMed  CAS  Google Scholar 

  55. Sergeeva OA, Doreulee N, Chepkova AN, Kazmierczak T, Haas HL (2007) Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur J NeuroSci 26:1889–1894

    Article  PubMed  CAS  Google Scholar 

  56. Singh S, Das T, Ravindran A, Chaturvedi RK, Shukla Y, Agarwal AK, Dikshit M (2005) Involvement of nitric oxide in neurodegeneration: a study on the experimental models of Parkinson’s disease. Redox Rep 10:103–109

    Article  PubMed  CAS  Google Scholar 

  57. Standaert DG, Friberg IK, Landwehrmeyer GB, Young AB, Penney JB Jr (1999) Expression of NMDA glutamate receptor subunit mRNAs in neurochemically identified projection and interneurons in the striatum of the rat. Brain Res Mol Brain Res 64:11–23

    Article  PubMed  CAS  Google Scholar 

  58. Surmeier DJ (2007) Calcium, ageing, and neuronal vulnerability in Parkinson’s disease. Lancet Neurol 6:933–938

    Article  PubMed  CAS  Google Scholar 

  59. Takahashi T (2005) Postsynaptic receptor mechanisms underlying developmental speeding of synaptic transmission. Neurosci Res 53:229–240

    Article  PubMed  CAS  Google Scholar 

  60. Tallaksen-Greene SJ, Kaatz KW, Romano C, Albin RL (1998) Localization of mGluR1a-like immunoreactivity and mGluR5-like immunoreactivity in identified populations of striatal neurons. Brain Res 780:210–217

    Article  PubMed  CAS  Google Scholar 

  61. Tepper JM, Sharpe NA, Koos TZ, Trent F (1998) Postnatal development of the rat neostriatum: electrophysiological, light- and electron-microscopic studies. Dev Neurosci 20:125–145

    Article  PubMed  CAS  Google Scholar 

  62. Tu JC, Xiao B, Naisbitt S, Yuan JP, Petralia RS, Brakeman P, Doan A, Aakalu VK, Lanahan AA, Sheng M, Worley PF (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23:583–592

    Article  PubMed  CAS  Google Scholar 

  63. Uchigashima M, Narushima M, Fukaya M, Katona I, Kano M, Watanabe M (2007) Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27:3663–3676

    Article  PubMed  CAS  Google Scholar 

  64. Wang Y (2008) Differential effect of aging on synaptic plasticity in the ventral and dorsal striatum. Neurobiol Learn Mem 89:70–75

    Article  PubMed  Google Scholar 

  65. Wang Z, Kai L, Day M, Ronesi J, Yin HH, Ding J, Tkatch T, Lovinger DM, Surmeier DJ (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50:443–452

    Article  PubMed  CAS  Google Scholar 

  66. Watanabe Y, Kato H, Araki T (2008) Protective action of neuronal nitric oxide synthase inhibitor in the MPTP mouse model of Parkinson’s disease. Metab Brain Dis 23:51–69

    Article  PubMed  CAS  Google Scholar 

  67. Wenzel A, Fritschy JM, Mohler H, Benke D (1997) NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469–478

    Article  PubMed  CAS  Google Scholar 

  68. Xiao B, Tu JC, Worley PF (2000) Homer: a link between neural activity and glutamate receptor function. Curr Opin Neurobiol 10:370–374

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Supported by DFG SE 1768, SFB 575/3, and 8.

Author information

Author notes

  1. Nanuli Doreulee

    Present address: Tbilisi State University, Georgia, USA

Authors and Affiliations

  1. Department of Neurophysiology, Heinrich-Heine-University, Dusseldorf, 40001, Germany

    Aisa N. Chepkova, Wiebke Fleischer, Thomas Kazmierczak, Nanuli Doreulee, Helmut L. Haas & Olga A. Sergeeva

Authors
  1. Aisa N. Chepkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wiebke Fleischer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Kazmierczak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nanuli Doreulee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Helmut L. Haas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Olga A. Sergeeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olga A. Sergeeva.

Additional information

Aisa N. Chepkova and Wiebke Fleischer contributed equally to the study.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00424-009-0732-5

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chepkova, A.N., Fleischer, W., Kazmierczak, T. et al. Developmental alterations of DHPG-induced long-term depression of corticostriatal synaptic transmission: switch from NMDA receptor-dependent towards CB1 receptor-dependent plasticity. Pflugers Arch - Eur J Physiol 459, 131–141 (2009). https://doi.org/10.1007/s00424-009-0714-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-009-0714-7

Keywords

Search

Navigation