Plastic Control of Striatal Glutamatergic Transmission by Ensemble Actions of Several Neurotransmitters and Targets for Drugs of Abuse
DAVID M. LOVINGER,
JOHN G. PARTRIDGE,
KA-CHOI TANG,
Corresponding Author
DAVID M. LOVINGER
Laboratory for Integrative Neuroscience, Division of Intramural Clinical and Basic Research, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, Maryland 20852, USA
Address for correspondence: Dr. David M. Lovinger, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20852. Voice: 301-443-2445; fax: 301-480-1734. [email protected]Search for more papers by this authorJOHN G. PARTRIDGE
Laboratory of Molecular Physiology, Division of Intramural Clinical and Basic Research, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, Maryland 20852, USA
Search for more papers by this authorKA-CHOI TANG
Ernest Gallo Clinic and Research Center, and the Department of Neurology, University of California at San Francisco, Emeryville, California 94608, USA
Search for more papers by this authorDAVID M. LOVINGER,
JOHN G. PARTRIDGE,
KA-CHOI TANG,
Corresponding Author
DAVID M. LOVINGER
Laboratory for Integrative Neuroscience, Division of Intramural Clinical and Basic Research, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, Maryland 20852, USA
Address for correspondence: Dr. David M. Lovinger, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20852. Voice: 301-443-2445; fax: 301-480-1734. [email protected]Search for more papers by this authorJOHN G. PARTRIDGE
Laboratory of Molecular Physiology, Division of Intramural Clinical and Basic Research, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Rockville, Maryland 20852, USA
Search for more papers by this authorKA-CHOI TANG
Ernest Gallo Clinic and Research Center, and the Department of Neurology, University of California at San Francisco, Emeryville, California 94608, USA
Search for more papers by this authorAbstract
Abstract: Long-lasting alterations in the efficacy of glutamatergic synapses, such as long-term potentiation (LTP) and long-term depression (LTD), are prominent models for mechanisms of information storage in the brain. It has been suggested that exposure to drugs of abuse produces synaptic plasticity at glutamatergic synapses that shares many features with LTP and LTD, and that these synaptic changes may play roles in addiction. We have examined the involvement of particular neurotransmitters in synaptic plasticity at glutamatergic synapses within the striatum, a brain region with prominent roles in initiation and sequencing of actions, as well as habit formation. Our studies indicate that multiple neurotransmitters interact to produce striatal synaptic plasticity, and that the relative strength and patterning of the afferent inputs that release the various neurotransmitters determines whether LTP or LTD is activated. Drugs of abuse interact with glutamatergic synaptic plasticity in multiple ways, including alterations in dopamine release and more direct effects on glutamate release and glutamate receptors. We hypothesize that these effects contribute to addiction by facilitating the formation of new, drug-centered habits, and by disruption of more adaptive behaviors.
REFERENCES
- 1 Nestler, E.J. 2001. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2: 119–128.
- 2 Gerdeman, G.L., J.G. Partridge, C.R. Lupica & D.M. Lovinger. 2003. It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci. 184–192.
- 3 Hyman, S.E. & R.C. Malenka. 2001. Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2: 695–703.
- 4 Schmidt, W.J. 1995. Balance of transmitter activities in the basal ganglia loops. J. Neural Transm. Suppl. 46: 67–76.
- 5 Tunstall, M.J., D.E. Oorschot, A. Kean & J.R. Wickens. 2002. Inhibitory interactions between spiny projection neurons in the rat striatum. J. Neurophysiol. 88: 1263–1269.
- 6 Czubayko, U. & D. Plenz. 2002. Fast synaptic transmission between striatal spiny projection neurons. Proc. Natl. Acad. Sci. USA 99: 15764–15769.
- 7 Kincaid, A.E., T. Zheng & C.J. Wilson. 1998. Connectivity and convergence of single corticostriatal axons. J. Neurosci. 18: 4722–4731.
- 8 Smith, Y., B.D. Bennett, J.P. Bolam, et al. 1994. Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J. Comp. Neurol. 344: 1–19.
- 9 Izzo, P.N. & J.P. Bolam. 1988. Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat. J. Comp. Neurol. 269: 219–234.
- 10 Bolam, J.P. & P.N. Izzo. 1988. The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons. Exp. Brain Res. 70: 361–377.
- 11 Koos, T. & J.M. Tepper. 1999. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 2: 467–472.
- 12 Koos, T. & J.M. Tepper. 2002. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J. Neurosci. 22: 529–535.
- 13 Wonnacott, S., S. Kaiser, A. Mogg, et al. 2000. Presynaptic nicotinic receptors modulating dopamine release in the rat striatum. Eur. J. Pharmacol. 393: 51–58.
- 14 Zhou, F.M., Y. Liang & J.A. Dani. 2001. Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4: 1224–1229.
- 15
Tarazi, F.I. & R.J. Baldessarini.
1999. Regional localization of dopamine and ionotropic glutamate receptor subtypes in striatolimbic brain regions.
J. Neurosci. Res.
55: 401–410.
10.1002/(SICI)1097-4547(19990215)55:4<401::AID-JNR1>3.0.CO;2-H CASPubMedWeb of Science®Google Scholar
- 16 Rouse, S.T., M.J. Marino, S.R. Bradley, et al. 2000. Distribution and roles of metabotropic glutamate receptors in the basal ganglia motor circuit: implications for treatment of Parkinson's disease and related disorders. Pharmacol. Ther. 88: 427–435.
- 17 Lovinger, D.M. & B.A. McCool. 1995. Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J. Neurophysiol. 73: 1076–1083.
- 18 Hersch, S.M., C.A. Gutekunst, H.D. Rees, et al. 1994. Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies. J. Neurosci. 14: 3351–3363.
- 19 Calabresi, P., N.B. Mercuri, M. De Murtas & G. Bernardi. 1991. Involvement of GABA systems in feedback regulation of glutamate- and GABA-mediated synaptic potentials in rat neostriatum. J. Physiol. 440: 581–599.
- 20 Bowen, W.D., S. Gentleman, M. Herkenham & C.B. Pert. 1981. Interconverting mu and delta forms of the opiate receptor in rat striatal patches. Proc. Natl. Acad. Sci. USA 78: 4818–4822.
- 21 Hohmann, A.G. & M. Herkenham. 2000. Localization of cannabinoid CB(1) receptor mRNA in neuronal subpopulations of rat striatum: a double-label in situ hybridization study. Synapse 37: 71–80.
- 22
Jiang, Z.G. & R.A. North.
1991. Membrane properties and synaptic responses of rat striatal neurones in vitro.
J. Physiol. (Lond.)
443: 533–553.
10.1113/jphysiol.1991.sp018850 Google Scholar
- 23 Malenka, R.C. & J.D. Kocsis. 1988. Presynaptic actions of carbachol and adenosine on corticostriatal synaptic transmission studied in vitro. J. Neurosci. 8: 3750–3756.
- 24 Gerdeman, G. & D.M. Lovinger. 2001. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 85: 468–471.
- 25 Huang, C.C., S.W. Lo & K.S. Hsu. 2001. Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J. Physiol. 532: 731–748.
- 26 Nicola, S.M., J. Surmeier & R.C. Malenka. 2000. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23: 185–215.
- 27 Aoyama, S., H. Kase & E. Borrelli. 2000. Rescue of locomotor impairment in dopamine D2 receptor-deficient mice by an adenosine A2A receptor antagonist. J. Neurosci. 20: 5848–5852.
- 28 Zahniser, N.R., J.K. Simosky, R.D. Mayfield, et al. 2000. Functional uncoupling of adenosine A(2A) receptors and reduced response to caffeine in mice lacking dopamine D2 receptors. J. Neurosci. 20: 5949–5957.
- 29 Chen, J.F., R. Moratalla, F. Impagnatiello, et al. 2001. The role of the D(2) dopamine receptor (D(2)R) in A(2A) adenosine receptor (A(2A)R)-mediated behavioral and cellular responses as revealed by A(2A) and D(2) receptor knockout mice. Proc. Natl. Acad. Sci. USA 98: 1970–1975.
- 30 Gonzalez, L.P. & E.H. Ellinwood, Jr. 1984. Cholinergic modulation of stimulant-induced behavior. Pharmacol. Biochem. Behav. 20: 397–403.
- 31 Costall, B. & R.J. Naylor. 1972. Modification of amphetamine effects by intracerebrally administered anticholinergic agents. Life Sci. I 11: 239–253.
- 32 Bickerdike, M.J. & E.D. Abercrombie. 1997. Striatal acetylcholine release correlates with behavioral sensitization in rats withdrawn from chronic amphetamine. J. Pharmacol. Exp. Ther. 282: 818–826.
- 33 Zhou, F.M., C.J. Wilson & J.A. Dani. 2002. Cholinergic interneuron characteristics and nicotinic properties in the striatum. J. Neurobiol. 53: 590–605.
- 34 Calabresi, P., R. Maj, A. Pisani, et al. 1992. Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J. Neurosci. 12: 4224–4233.
- 35 Calabresi, P., P. Gubellini, D. Centonze, et al. 1999. A critical role of the nitric oxide/cGMP pathway in corticostriatal long-term depression. J. Neurosci. 19: 2489–2499.
- 36 Battaglia, G., V. Bruno, A. Pisani, et al. 2001. Selective blockade of type-1 metabotropic glutamate receptors induces neuroprotection by enhancing gabaergic transmission. Mol. Cell. Neurosci. 17: 1071–1083.
- 37 Sung, K.W., S. Choi & D.M. Lovinger. 2001. Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J. Neurophysiol. 86: 2405–2412.
- 38
Testa, C.M. I.K. Friberg, S.W. Weiss & D.G. Standaert.
1998. Immunohistochemical localization of metabotropic glutamate receptors mGluR1a and mGluR2/3 in the rat basal ganglia.
J. Comp. Neurol.
390: 5–19.
10.1002/(SICI)1096-9861(19980105)390:1<5::AID-CNE2>3.0.CO;2-6 CASPubMedWeb of Science®Google Scholar
- 39 Spencer, J.P. & K.P. Murphy. 2000. Bi-directional changes in synaptic plasticity induced at corticostriatal synapses in vitro. Exp. Brain Res. 135: 497–503.
- 40 Choi, S. & D.M. Lovinger. 1997. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc. Natl. Acad. Sci. USA 94: 2665–2670.
- 41 Partridge, J.G., S. Apparsundaram, G.A. Gerhardt, et al. 2002. Nicotinic acetylcholine receptors interact with dopamine in induction of striatal long-term depression. J. Neurosci. 22: 2541–2549.
- 42 Gerdeman, G.L., J. Ronesi & D.M. Lovinger. 2002. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5: 446–451.
- 43 Robbe, D., M. Kopf, A. Remaury, et al. 2002. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 99: 8384–8388.
- 44 Marsicano, G., C.T. Wotjak, S.C. Azad, et al. 2002. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418: 530–534.
- 45 Partridge, J.G., K.C. Tang & D.M. Lovinger. 2000. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J. Neurophysiol. 84: 1422–1429.
- 46 Calabresi, P., A. Pisani, N.B. Mercuri & G. Bernardi. 1992. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur. J. Neurosci. 4: 929–935.
- 47 Centonze, D., B. Picconi, P. Gubellini, et al. 2001. Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur. J. Neurosci. 13: 1071–1077.
- 48 Kerr, J.N. & J.R. Wickens. 2001. Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J. Neurophysiol. 85: 117–124.
- 49 Calabresi, P., D. Centonze, P. Gubellini & G. Bernardi. 1999. Activation of M1-like muscarinic receptors is required for the induction of corticostriatal LTP. Neuropharmacology 38: 323–326.
- 50 Huang, Y.Y. & E.R. Kandel. 1995. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus [see comments]. Proc. Natl. Acad. Sci. USA 92: 2446–2450.
- 51 Hersch, S.M., B.J. Ciliax, C.A. Gutekunst, et al. 1995. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J. Neurosci. 15: 5222–5237.
- 52 Flores-Hernandez, J., C. Cepeda, E. Hernandez-Echeagaray, et al. 2002. Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J. Neurophysiol. 88: 3010–3020.
- 53 Hersch, S.M. & A.I. Levey. 1995. Diverse pre- and post-synaptic expression of m1-m4 muscarinic receptor proteins in neurons and afferents in the rat neostriatum. Life Sci. 56: 931–938.
- 54 Reynolds, J.N. & J.R. Wickens. 2002. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw. 15: 507–521.
- 55 Lujan, R., J.D. Roberts, R. Shigemoto, et al. 1997. Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1 alpha, mGluR2 and mGluR5, relative to neurotransmitter release sites. J. Chem. Neuroanat. 13: 219–241.
- 56 Richfield, E.K., J.B. Penney & A.B. Young. 1989. Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience 30: 767–777.
- 57 Wilson, C.J. & Y. Kawaguchi. 1996. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16: 2397–2410.
- 58 Schultz, W. 2002. Getting formal with dopamine and reward. Neuron 36: 241–263.
- 59 Bennett, B.D. & C.J. Wilson. 1999. Spontaneous activity of neostriatal cholinergic interneurons in vitro. J. Neurosci. 19: 5586–5596.
- 60 Kombian, S.B. & R.C. Malenka. 1994. Simultaneous LTP of non-NMDA- and LTD of NMDA-receptor-mediated responses in the nucleus accumbens. Nature 368: 242–246.
- 61 Graybiel, A.M. 1998. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70: 119–136.
- 62 Nicola, S.M. & R.C. Malenka. 1998. Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J. Neurophysiol. 79: 1768–1776.
- 63 Everitt, B.J. & M.E. Wolf. 2002. Psychomotor stimulant addiction: a neural systems perspective. J. Neurosci. 22: 3312–3320.
- 64 Broberger, C., D. Blacker, L. Gimenez-Llort, et al. 1998. Modulation of motor behaviour by NMDA- and cholecystokinin-antagonism. Amino Acids 14: 25–31.
- 65 Schmidt, W.J. & B.D. Kretschmer. 1997. Behavioural pharmacology of glutamate receptors in the basal ganglia. Neurosci. Biobehav. Rev. 21: 381–392.
- 66 Gough, A.L. & J.E. Olley. 1978. Catalepsy induced by intrastriatal injections of delta9-THC and 11-OH- delta9-THC in the rat. Neuropharmacology 17: 137–144.
- 67 Packard, M.G. & B.J. Knowlton. 2002. Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25: 563–593.
- 68 Chang, Q. & P.E. Gold. 2003. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J. Neurosci. 23: 3001–3005.
- 69 Jog, M.S., Y. Kubota, C.I. Connolly, et al. 1999. Building neural representations of habits. Science 286: 1745–1749.
- 70 Graybiel, A.M. & S.L. Rauch. 2000. Toward a neurobiology of obsessive-compulsive disorder. Neuron 28: 343–347.
Citing Literature
