Accessible Requires Authentication Published by De Gruyter July 19, 2014

Long-term depression at distinct glutamatergic synapses in the basal ganglia

Julien P. Dupuis, Bernard H. Bioulac and Jérôme Baufreton

Abstract

Long-term adaptations of synaptic transmission are believed to be the cellular basis of information storage in the brain. In particular, long-term depression of excitatory neurotransmission has been under intense investigation since convergent lines of evidence support a crucial role for this process in learning and memory. Within the basal ganglia, a network of subcortical nuclei forming a key part of the extrapyramidal motor system, plasticity at excitatory synapses is essential to the regulation of motor, cognitive, and reward functions. The striatum, the main gateway of the basal ganglia, receives convergent excitatory inputs from cortical areas and transmits information to the network output structures and is a major site of activity-dependent plasticity. Indeed, long-term depression at cortico-striatal synapses modulates the transfer of information to basal ganglia output structures and affects voluntary movement execution. Cortico-striatal plasticity is thus considered as a cellular substrate for adaptive motor control. Downstream in this network, the subthalamic nucleus and substantia nigra nuclei also receive glutamatergic innervation from the cortex and the subthalamic nucleus, respectively. Although these connections have been less investigated, recent studies have started to unravel the molecular mechanisms that contribute to adjustments in the strength of cortico-subthalamic and subthalamo-nigral transmissions, revealing that adaptations at these synapses governing the output of the network could also contribute to motor planning and execution. Here, we review our current understanding of long-term depression mechanisms at basal ganglia glutamatergic synapses and emphasize the common and unique plastic features observed at successive levels of the network in healthy and pathological conditions.


Corresponding author: Jérôme Baufreton, Université Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, 146 rue Léo Saignat, F-33000 Bordeaux, France, e-mail: ; and CNRS, Institut des Maladies Neurodégénératives, UMR 5293, F-33000 Bordeaux, France

Acknowledgments

This work was supported by Agence Nationale pour la Recherche (grant no. ANR-08-MNPS-035), Centre National de la Recherche Scientifique, the region Aquitaine, the ERA-NET Neuron 2nd Call for transnational research projects 2009 (grant no. 2009 NEUR 005 03), and the Labex Brain (ANR-10-LABX-0043).

References

Aceves, J.J., Rueda-Orozco, P.E., Hernandez-Martinez, R., Galarraga, E., and Bargas, J. (2011). Bidirectional plasticity in striatonigral synapses: a switch to balance direct and indirect basal ganglia pathways. Learn. Mem. 18, 764–773. Search in Google Scholar

Ade, K.K. and Lovinger, D.M. (2007). Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J. Neurosci. 27, 2403–2409. Search in Google Scholar

Adermark, L. and Lovinger, D.M. (2007a). Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc. Natl. Acad. Sci. USA 104, 20564–20569. Search in Google Scholar

Adermark, L. and Lovinger, D.M. (2007b). Combined activation of L-type Ca2+ channels and synaptic transmission is sufficient to induce striatal long-term depression. J. Neurosci. 27, 6781–6787. Search in Google Scholar

Albin, R.L. (1995). The pathophysiology of chorea/ballism and Parkinsonism. Parkinsonism Relat. Disord. 1, 3–11. Search in Google Scholar

Alexander, G.E. and Crutcher, M.D. (1990). Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266–271. Search in Google Scholar

Alexander, G.E., DeLong, M.R., and Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381. Search in Google Scholar

Arcangeli, S., Tozzi, A., Tantucci, M., Spaccatini, C., de Iure, A., Costa, C., Di Filippo, M., Picconi, B., Giampa, C., Fusco, F.R., et al. (2013). Ischemic-LTP in striatal spiny neurons of both direct and indirect pathway requires the activation of D1-like receptors and NO/soluble guanylate cyclase/cGMP transmission. J. Cereb. Blood Flow Metab. 33, 278–286. Search in Google Scholar

Atherton, J.F. and Bevan, M.D. (2005). Ionic mechanisms underlying autonomous action potential generation in the somata and dendrites of GABAergic substantia nigra pars reticulata neurons in vitro. J. Neurosci. 25, 8272–8281. Search in Google Scholar

Atwood, B.K., Kupferschmidt, D.A., and Lovinger, D.M. (2014). Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum. Nat. Neurosci. 17, 540–548. Search in Google Scholar

Bagetta, V., Picconi, B., Marinucci, S., Sgobio, C., Pendolino, V., Ghiglieri, V., Fusco, F.R., Giampa, C., and Calabresi, P. (2011). Dopamine-dependent long-term depression is expressed in striatal spiny neurons of both direct and indirect pathways: implications for Parkinson’s disease. J. Neurosci. 31, 12513–12522. Search in Google Scholar

Balleine, B.W., Delgado, M.R., and Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. J. Neurosci. 27, 8161–8165. Search in Google Scholar

Bar-Gad, I., Elias, S., Vaadia, E., and Bergman, H. (2004). Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J. Neurosci. 24, 7410–7419. Search in Google Scholar

Bartlett, T.E., Bannister, N.J., Collett, V.J., Dargan, S.L., Massey, P.V., Bortolotto, Z.A., Fitzjohn, S.M., Bashir, Z.I., Collingridge, G.L., and Lodge, D. (2007). Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology 52, 60–70. Search in Google Scholar

Belluscio, M.A., Kasanetz, F., Riquelme, L.A., and Murer, M.G. (2003). Spreading of slow cortical rhythms to the basal ganglia output nuclei in rats with nigrostriatal lesions. Eur. J. Neurosci. 17, 1046–1052. Search in Google Scholar

Benazzouz, A., Gross, C., Feger, J., Boraud, T., and Bioulac, B. (1993). Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur. J. Neurosci. 5, 382–389. Search in Google Scholar

Bergman, H., Wichmann, T., and DeLong, M.R. (1990). Reversal of experimental Parkinsonism by lesions of the subthalamic nucleus. Science 249, 1436–1438. Search in Google Scholar

Bergman, H., Wichmann, T., Karmon, B., and DeLong, M.R. (1994). The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of Parkinsonism. J. Neurophysiol. 72, 507–520. Search in Google Scholar

Bertran-Gonzalez, J., Herve, D., Girault, J.A., and Valjent, E. (2010). What is the degree of segregation between striatonigral and striatopallidal projections? Front. Neuroanat. 4, 1–9. Search in Google Scholar

Blythe, S.N., Wokosin, D., Atherton, J.F., and Bevan, M.D. (2009). Cellular mechanisms underlying burst firing in substantia nigra dopamine neurons. J. Neurosci. 29, 15531–15541. Search in Google Scholar

Bonifati, V. (2007). Genetics of Parkinsonism. Parkinsonism Relat. Disord. 13(suppl 3), S233–S241. Search in Google Scholar

Bonsi, P., Martella, G., Cuomo, D., Platania, P., Sciamanna, G., Bernardi, G., Wess, J., and Pisani, A. (2008). Loss of muscarinic autoreceptor function impairs long-term depression but not long-term potentiation in the striatum. J. Neurosci. 28, 6258–6263. Search in Google Scholar

Bradfield, L.A., Bertran-Gonzalez, J., Chieng, B., and Balleine, B.W. (2013). The thalamostriatal pathway and cholinergic control of goal-directed action: interlacing new with existing learning in the striatum. Neuron 79, 153–166. Search in Google Scholar

Brazhnik, E., Cruz, A.V., Avila, I., Wahba, M.I., Novikov, N., Ilieva, N.M., McCoy, A.J., Gerber, C., and Walters, J.R. (2012). State-dependent spike and local field synchronization between motor cortex and substantia nigra in hemiparkinsonian rats. J. Neurosci. 32, 7869–7880. Search in Google Scholar

Calabresi, P., Maj, R., Mercuri, N.B., and Bernardi, G. (1992a). Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci. Lett. 142, 95–99. Search in Google Scholar

Calabresi, P., Pisani, A., Mercuri, N.B., and Bernardi, G. (1992b). 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. Search in Google Scholar

Calabresi, P., Maj, R., Pisani, A., Mercuri, N.B., and Bernardi, G. (1992c). Long-term synaptic depression in the striatum: physiological and pharmacological characterization. J. Neurosci. 12, 4224–4233. Search in Google Scholar

Calabresi, P., Saiardi, A., Pisani, A., Baik, J.H., Centonze, D., Mercuri, N.B., Bernardi, G., and Borrelli, E. (1997). Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J. Neurosci. 17, 4536–4544. Search in Google Scholar

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

Calabresi, P., Picconi, B., Tozzi, A., and Di Filippo, M. (2007). Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci. 30, 211–219. Search in Google Scholar

Centonze, D., Grande, C., Saulle, E., Martin, A.B., Gubellini, P., Pavon, N., Pisani, A., Bernardi, G., Moratalla, R., and Calabresi, P. (2003). Distinct roles of D1 and D5 dopamine receptors in motor activity and striatal synaptic plasticity. J. Neurosci. 23, 8506–8512. Search in Google Scholar

Charpier, S. and Deniau, J.M. (1997). In vivo activity-dependent plasticity at cortico-striatal connections: evidence for physiological long-term potentiation. Proc. Natl. Acad. Sci. USA 94, 7036–7040. Search in Google Scholar

Chevalier, G. and Deniau, J.M. (1990). Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277–280. Search in Google Scholar

Choi, S. and Lovinger, D.M. (1997a). Decreased frequency but not amplitude of quantal synaptic responses associated with expression of corticostriatal long-term depression. J. Neurosci. 17, 8613–8620. Search in Google Scholar

Choi, S. and Lovinger, D.M. (1997b). Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc. Natl. Acad. Sci. USA 94, 2665–2670. Search in Google Scholar

Chou, J.S., Chen, C.Y., Chen, Y.L., Weng, Y.H., Yeh, T.H., Lu, C.S., Chang, Y.M., and Wang, H.L. (2014). (G2019S) LRRK2 causes early-phase dysfunction of SNpc dopaminergic neurons and impairment of corticostriatal long-term depression in the PD transgenic mouse. Neurobiol. Dis. 68C, 190–199. Search in Google Scholar

Cui, G., Jun, S.B., Jin, X., Pham, M.D., Vogel, S.S., Lovinger, D.M., and Costa, R.M. (2013). Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494, 238–242. Search in Google Scholar

de Jesus Aceves, J., Rueda-Orozco, P.E., Hernandez, R., Plata, V., Ibanez-Sandoval, O., Galarraga, E., and Bargas, J. (2011). Dopaminergic presynaptic modulation of nigral afferents: its role in the generation of recurrent bursting in substantia nigra pars reticulata neurons. Front. Syst. Neurosci. 5, 6. Search in Google Scholar

DeLong, M.R. (1990). Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281–285. Search in Google Scholar

Deniau, J.M., Mailly, P., Maurice, N., and Charpier, S. (2007). The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog. Brain Res. 160, 151–172. Search in Google Scholar

Ding, J.B., Guzman, J.N., Peterson, J.D., Goldberg, J.A., and Surmeier, D.J. (2010). Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67, 294–307. Search in Google Scholar

Dupuis, J.P., Feyder, M., Miguelez, C., Garcia, L., Morin, S., Choquet, D., Hosy, E., Bezard, E., Fisone, G., Bioulac, B.H., et al. (2013). Dopamine-dependent long-term depression at subthalamo-nigral synapses is lost in experimental Parkinsonism. J. Neurosci. 33, 14331–14341. Search in Google Scholar

Ellender, T.J., Harwood, J., Kosillo, P., Capogna, M., and Bolam, J.P. (2013). Heterogeneous properties of central lateral and parafascicular thalamic synapses in the striatum. J. Physiol. 591, 257–272. Search in Google Scholar

Fino, E., Glowinski, J., and Venance, L. (2005). Bidirectional activity-dependent plasticity at corticostriatal synapses. J. Neurosci. 25, 11279–11287. Search in Google Scholar

Gardoni, F., Mauceri, D., Malinverno, M., Polli, F., Costa, C., Tozzi, A., Siliquini, S., Picconi, B., Cattabeni, F., Calabresi, P., et al. (2009). Decreased NR2B subunit synaptic levels cause impaired long-term potentiation but not long-term depression. J. Neurosci. 29, 669–677. Search in Google Scholar

Gerdeman, G.L., Ronesi, J., and Lovinger, D.M. (2002). Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5, 446–451. Search in Google Scholar

Gerfen, C.R., Engber, T.M., Mahan, L.C., Susel, Z., Chase, T.N., Monsma, F.J., Jr., and Sibley, D.R. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429–1432. Search in Google Scholar

Gertler, T.S., Chan, C.S., and Surmeier, D.J. (2008). Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 28, 10814–10824. Search in Google Scholar

Gittis, A.H., Hang, G.B., LaDow, E.S., Shoenfeld, L.R., Atallah, B.V., Finkbeiner, S., and Kreitzer, A.C. (2011). Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 71, 858–868. Search in Google Scholar

Giuffrida, A., Parsons, L.H., Kerr, T.M., Rodriguez de Fonseca, F., Navarro, M., and Piomelli, D. (1999). Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat. Neurosci. 2, 358–363. Search in Google Scholar

Goldberg, M.S., Pisani, A., Haburcak, M., Vortherms, T.A., Kitada, T., Costa, C., Tong, Y., Martella, G., Tscherter, A., Martins, A., et al. (2005). Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 45, 489–496. Search in Google Scholar

Graybiel, A.M. (2005). The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 15, 638–644. Search in Google Scholar

Gubellini, P., Saulle, E., Centonze, D., Bonsi, P., Pisani, A., Bernardi, G., Conquet, F., and Calabresi, P. (2001). Selective involvement of mGlu1 receptors in corticostriatal LTD. Neuropharmacology 40, 839–846. Search in Google Scholar

Gureviciene, I., Gurevicius, K., and Tanila, H. (2009). Aging and alpha-synuclein affect synaptic plasticity in the dentate gyrus. J. Neural Transm. 116, 13–22. Search in Google Scholar

Guridi, J., Herrero, M.T., Luquin, M.R., Guillen, J., Ruberg, M., Laguna, J., Vila, M., Javoy-Agid, F., Agid, Y., Hirsch, E., et al. (1996). Subthalamotomy in parkinsonian monkeys. Behavioural and biochemical analysis. Brain 119(pt 5), 1717–1727. Search in Google Scholar

Haber, S.N. and Calzavara, R. (2009). The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res. Bull. 78, 69–74. Search in Google Scholar

Harnett, M.T., Bernier, B.E., Ahn, K.C., and Morikawa, H. (2009). Burst-timing-dependent plasticity of NMDA receptor-mediated transmission in midbrain dopamine neurons. Neuron 62, 826–838. Search in Google Scholar

Henderson, J.M., Carpenter, K., Cartwright, H., and Halliday, G.M. (2000). Loss of thalamic intralaminar nuclei in progressive supranuclear palsy and Parkinson’s disease: clinical and therapeutic implications. Brain 123(pt 7), 1410–1421. Search in Google Scholar

Hutchison, W.D., Allan, R.J., Opitz, H., Levy, R., Dostrovsky, J.O., Lang, A.E., and Lozano, A.M. (1998). Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Ann. Neurol. 44, 622–628. Search in Google Scholar

Ibanez-Sandoval, O., Hernandez, A., Floran, B., Galarraga, E., Tapia, D., Valdiosera, R., Erlij, D., Aceves, J., and Bargas, J. (2006). Control of the subthalamic innervation of substantia nigra pars reticulata by D1 and D2 dopamine receptors. J. Neurophysiol. 95, 1800–1811. Search in Google Scholar

Johnson, K.A., Niswender, C.M., Conn, P.J., and Xiang, Z. (2011). Activation of group II metabotropic glutamate receptors induces long-term depression of excitatory synaptic transmission in the substantia nigra pars reticulata. Neurosci. Lett. 504, 102–106. Search in Google Scholar

Jouve, L., Salin, P., Melon, C., and Kerkerian-Le Goff, L. (2010). Deep brain stimulation of the center median-parafascicular complex of the thalamus has efficient anti-parkinsonian action associated with widespread cellular responses in the basal ganglia network in a rat model of Parkinson’s disease. J. Neurosci. 30, 9919–9928. Search in Google Scholar

Kheirbek, M.A., Britt, J.P., Beeler, J.A., Ishikawa, Y., McGehee, D.S., and Zhuang, X. (2009). Adenylyl cyclase type 5 contributes to corticostriatal plasticity and striatum-dependent learning. J. Neurosci. 29, 12115–12124. Search in Google Scholar

Kitada, T., Pisani, A., Porter, D.R., Yamaguchi, H., Tscherter, A., Martella, G., Bonsi, P., Zhang, C., Pothos, E.N., and Shen, J. (2007). Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl. Acad. Sci. USA 104, 11441–11446. Search in Google Scholar

Kitada, T., Pisani, A., Karouani, M., Haburcak, M., Martella, G., Tscherter, A., Platania, P., Wu, B., Pothos, E.N., and Shen, J. (2009). Impaired dopamine release and synaptic plasticity in the striatum of parkin-/- mice. J. Neurochem. 110, 613–621. Search in Google Scholar

Klein, C., Lohmann-Hedrich, K., Rogaeva, E., Schlossmacher, M.G., and Lang, A.E. (2007). Deciphering the role of heterozygous mutations in genes associated with Parkinsonism. Lancet neurology 6, 652–662. Search in Google Scholar

Kramer, P.F., Christensen, C.H., Hazelwood, L.A., Dobi, A., Bock, R., Sibley, D.R., Mateo, Y., and Alvarez, V.A. (2011). Dopamine D2 receptor overexpression alters behavior and physiology in Drd2-EGFP mice. J. Neurosci. 31, 126–132. Search in Google Scholar

Kravitz, A.V., Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K., and Kreitzer, A.C. (2010). Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622–626. Search in Google Scholar

Kreitzer, A.C. and Malenka, R.C. (2005). Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 25, 10537–10545. Search in Google Scholar

Kreitzer, A.C. and Malenka, R.C. (2007). Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature 445, 643–647. Search in Google Scholar

Kreitzer, A.C. and Malenka, R.C. (2008). Striatal plasticity and basal ganglia circuit function. Neuron 60, 543–554. Search in Google Scholar

Lee, K.W., Hong, J.H., Choi, I.Y., Che, Y., Lee, J.K., Yang, S.D., Song, C.W., Kang, H.S., Lee, J.H., Noh, J.S., et al. (2002). Impaired D2 dopamine receptor function in mice lacking type 5 adenylyl cyclase. J. Neurosci. 22, 7931–7940. Search in Google Scholar

Lerner, T.N. and Kreitzer, A.C. (2011). Neuromodulatory control of striatal plasticity and behavior. Curr. Opin. Neurobiol. 21, 322–327. Search in Google Scholar

Lerner, T.N. and Kreitzer, A.C. (2012). RGS4 is required for dopaminergic control of striatal LTD and susceptibility to parkinsonian motor deficits. Neuron 73, 347–359. Search in Google Scholar

Lerner, T.N., Horne, E.A., Stella, N., and Kreitzer, A.C. (2010). Endocannabinoid signaling mediates psychomotor activation by adenosine A2A antagonists. J. Neurosci. 30, 2160–2164. Search in Google Scholar

Levy, R., Hutchison, W.D., Lozano, A.M., and Dostrovsky, J.O. (2000). High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J. Neurosci. 20, 7766–7775. Search in Google Scholar

Li, X., Patel, J.C., Wang, J., Avshalumov, M.V., Nicholson, C., Buxbaum, J.D., Elder, G.A., Rice, M.E., and Yue, Z. (2010). Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson’s disease mutation G2019S. J. Neurosci. 30, 1788–1797. Search in Google Scholar

Limousin, P., Pollak, P., Benazzouz, A., Hoffmann, D., Le Bas, J.F., Broussolle, E., Perret, J.E., and Benabid, A.L. (1995). Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345, 91–95. Search in Google Scholar

Litvak, V., Jha, A., Eusebio, A., Oostenveld, R., Foltynie, T., Limousin, P., Zrinzo, L., Hariz, M.I., Friston, K., and Brown, P. (2011). Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson’s disease. Brain 134, 359–374. Search in Google Scholar

Liu, L., Wong, T.P., Pozza, M.F., Lingenhoehl, K., Wang, Y., Sheng, M., Auberson, Y.P., and Wang, Y.T. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021–1024. Search in Google Scholar

Luscher, C. and Malenka, R.C. (2011). Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650–663. Search in Google Scholar

Madeo, G., Martella, G., Schirinzi, T., Ponterio, G., Shen, J., Bonsi, P., and Pisani, A. (2012). Aberrant striatal synaptic plasticity in monogenic Parkinsonisms. Neuroscience 211, 126–135. Search in Google Scholar

Magill, P.J., Sharott, A., Bevan, M.D., Brown, P., and Bolam, J.P. (2004). Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J. Neurophysiol. 92, 700–714. Search in Google Scholar

Mallet, N., Ballion, B., Le Moine, C., and Gonon, F. (2006). Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 26, 3875–3884. Search in Google Scholar

Mallet, N., Pogosyan, A., Marton, L.F., Bolam, J.P., Brown, P., and Magill, P.J. (2008a). Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J. Neurosci. 28, 14245–14258. Search in Google Scholar

Mallet, N., Pogosyan, A., Sharott, A., Csicsvari, J., Bolam, J.P., Brown, P., and Magill, P.J. (2008b). Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J. Neurosci. 28, 4795–4806. Search in Google Scholar

Mathur, B.N. and Lovinger, D.M. (2012). Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front. Pharmacol. 3, 66. Search in Google Scholar

Matsumoto, N., Minamimoto, T., Graybiel, A.M., and Kimura, M. (2001). Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85, 960–976. Search in Google Scholar

Maurice, N., Deniau, J.M., Glowinski, J., and Thierry, A.M. (1998). Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J. Neurosci. 18, 9539–9546. Search in Google Scholar

Mazzone, P., Stocchi, F., Galati, S., Insola, A., Altibrandi, M.G., Modugno, N., Tropepi, D., Brusa, L., and Stefani, A. (2006). Bilateral implantation of centromedian-parafascicularis complex and GPi: a new combination of unconventional targets for deep brain stimulation in severe Parkinson disease. Neuromodulation 9, 221–228. Search in Google Scholar

Melrose, H.L., Dächsel, J.C., Behrouz, B., Lincoln, S.J., Yue, M., Hinkle, K.M., Kent, C.B., Korvatska, E., Taylor, J.P., Witten, L., et al. (2010). Impaired dopaminergic neurotransmission and microtubule-associated protein tau alterations in human LRRK2 transgenic mice. Neurobiol. Dis. 40, 503–517. Search in Google Scholar

Minamimoto, T., Hori, Y., and Kimura, M. (2005). Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308, 1798–1801. Search in Google Scholar

Missale, C., Nash, S.R., Robinson, S.W., Jaber, M., and Caron, M.G. (1998). Dopamine receptors: from structure to function. Physiol. Rev. 78, 189–225. Search in Google Scholar

Montague, P.R., Hyman, S.E., and Cohen, J.D. (2004). Computational roles for dopamine in behavioural control. Nature 431, 760–767. Search in Google Scholar

Muller, T., Albrecht, D., and Gebhardt, C. (2009). Both NR2A and NR2B subunits of the NMDA receptor are critical for long-term potentiation and long-term depression in the lateral amygdala of horizontal slices of adult mice. Learn. Mem. 16, 395–405. Search in Google Scholar

Murer, M.G., Riquelme, L.A., Tseng, K.Y., and Pazo, J.H. (1997). Substantia nigra pars reticulata single unit activity in normal and 60HDA-lesioned rats: effects of intrastriatal apomorphine and subthalamic lesions. Synapse 27, 278–293. Search in Google Scholar

Nambu, A., Takada, M., Inase, M., and Tokuno, H. (1996). Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J. Neurosci. 16, 2671–2683. Search in Google Scholar

Nanda, B., Galvan, A., Smith, Y., and Wichmann, T. (2009). Effects of stimulation of the centromedian nucleus of the thalamus on the activity of striatal cells in awake rhesus monkeys. Eur. J. Neurosci. 29, 588–598. Search in Google Scholar

Nazzaro, C., Greco, B., Cerovic, M., Baxter, P., Rubino, T., Trusel, M., Parolaro, D., Tkatch, T., Benfenati, F., Pedarzani, P., et al. (2012). SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance. Nat. Neurosci. 15, 284–293. Search in Google Scholar

Obeso, J.A., Rodriguez-Oroz, M.C., Rodriguez, M., Lanciego, J.L., Artieda, J., Gonzalo, N., and Olanow, C.W. (2000). Pathophysiology of the basal ganglia in Parkinson’s disease. Trends Neurosci. 23, S8–S19. Search in Google Scholar

Oh, J.D., Russell, D.S., Vaughan, C.L., and Chase, T.N. (1998). Enhanced tyrosine phosphorylation of striatal NMDA receptor subunits: effect of dopaminergic denervation and L-DOPA administration. Brain Res. 813, 150–159. Search in Google Scholar

Oh, J.D., Vaughan, C.L., and Chase, T.N. (1999). Effect of dopamine denervation and dopamine agonist administration on serine phosphorylation of striatal NMDA receptor subunits. Brain Res. 821, 433–442. Search in Google Scholar

Overton, P.G., Richards, C.D., Berry, M.S., and Clark, D. (1999). Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. NeuroReport 10, 221–226. Search in Google Scholar

Packard, M.G. and Knowlton, B.J. (2002). Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25, 563–593. Search in Google Scholar

Paille, V., Picconi, B., Bagetta, V., Ghiglieri, V., Sgobio, C., Di Filippo, M., Viscomi, M.T., Giampa, C., Fusco, F.R., Gardoni, F., et al. (2010). Distinct levels of dopamine denervation differentially alter striatal synaptic plasticity and NMDA receptor subunit composition. J. Neurosci. 30, 14182–14193. Search in Google Scholar

Paille, V., Fino, E., Du, K., Morera-Herreras, T., Perez, S., Kotaleski, J.H., and Venance, L. (2013). GABAergic circuits control spike-timing-dependent plasticity. J. Neurosci. 33, 9353–9363. Search in Google Scholar

Picconi, B., Pisani, A., Centonze, D., Battaglia, G., Storto, M., Nicoletti, F., Bernardi, G., and Calabresi, P. (2002). Striatal metabotropic glutamate receptor function following experimental Parkinsonism and chronic levodopa treatment. Brain 125, 2635–2645. Search in Google Scholar

Picconi, B., Centonze, D., Hakansson, K., Bernardi, G., Greengard, P., Fisone, G., Cenci, M.A., and Calabresi, P. (2003). Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat. Neurosci. 6, 501–506. Search in Google Scholar

Picconi, B., Centonze, D., Rossi, S., Bernardi, G., and Calabresi, P. (2004). Therapeutic doses of L-dopa reverse hypersensitivity of corticostriatal D2-dopamine receptors and glutamatergic overactivity in experimental Parkinsonism. Brain 127, 1661–1669. Search in Google Scholar

Prescott, I.A., Dostrovsky, J.O., Moro, E., Hodaie, M., Lozano, A.M., and Hutchison, W.D. (2009). Levodopa enhances synaptic plasticity in the substantia nigra pars reticulata of Parkinson’s disease patients. Brain 132, 309–318. Search in Google Scholar

Quintana, A., Sgambato-Faure, V., and Savasta, M. (2012). Effects of L-DOPA and STN-HFS dyskinesiogenic treatments on NR2B regulation in basal ganglia in the rat model of Parkinson’s disease. Neurobiol. Dis. 48, 379–390. Search in Google Scholar

Radnikow, G. and Misgeld, U. (1998). Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J. Neurosci. 18, 2009–2016. Search in Google Scholar

Raz, A., Frechter-Mazar, V., Feingold, A., Abeles, M., Vaadia, E., and Bergman, H. (2001). Activity of pallidal and striatal tonically active neurons is correlated in MPTP-treated monkeys but not in normal monkeys. J. Neurosci. 21, RC128. Search in Google Scholar

Reynolds, J.N. and Wickens, J.R. (2000). Substantia nigra dopamine regulates synaptic plasticity and membrane potential fluctuations in the rat neostriatum, in vivo. Neuroscience 99, 199–203. Search in Google Scholar

Robertson, G.S. and Robertson, H.A. (1988). Evidence that the substantia nigra is a site of action for L-DOPA. Neurosci. Lett. 89, 204–208. Search in Google Scholar

Robertson, G.S. and Robertson, H.A. (1989). Evidence that L-DOPA-induced rotational behavior is dependent on both striatal and nigral mechanisms. J. Neurosci. 9, 3326–3331. Search in Google Scholar

Ronesi, J. and Lovinger, D.M. (2005). Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J. Physiol. 562, 245–256. Search in Google Scholar

Ronesi, J., Gerdeman, G.L., and Lovinger, D.M. (2004). Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J. Neurosci. 24, 1673–1679. Search in Google Scholar

Sano, H., Chiken, S., Hikida, T., Kobayashi, K., and Nambu, A. (2013). Signals through the striatopallidal indirect pathway stop movements by phasic excitation in the substantia nigra. J. Neurosci. 33, 7583–7594. Search in Google Scholar

Schmidt, R., Leventhal, D.K., Mallet, N., Chen, F., and Berke, J.D. (2013). Canceling actions involves a race between basal ganglia pathways. Nat. Neurosci. 16, 1118–1124. Search in Google Scholar

Schultz, W. (1998). Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1–27. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (1997). Presynaptic GABAB and adenosine A1 receptors regulate synaptic transmission to rat substantia nigra reticulata neurones. J. Physiol. 505 (Pt 1), 153–163. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2000). Presynaptic dopamine D2 and muscarine M3 receptors inhibit excitatory and inhibitory transmission to rat subthalamic neurones in vitro. J. Physiol. 525(pt 2), 331–341. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2001). Presynaptic GABA(B) receptors inhibit synaptic inputs to rat subthalamic neurons. Neuroscience 108, 431–436. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2002). Presynaptic modulation of synaptic transmission by opioid receptor in rat subthalamic nucleus in vitro. J. Physiol. 541, 219–230. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2003a). Group II metabotropic glutamate receptor modulation of excitatory transmission in rat subthalamic nucleus. J. Physiol. 553, 489–496. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2003b). Presynaptic inhibition of synaptic transmission by adenosine in rat subthalamic nucleus in vitro. Neuroscience 116, 99–106. Search in Google Scholar

Shen, K.Z. and Johnson, S.W. (2008). 5-HT inhibits synaptic transmission in rat subthalamic nucleus neurons in vitro. Neuroscience 151, 1029–1033. Search in Google Scholar

Shen, K.Z., Zhu, Z.T., Munhall, A., and Johnson, S.W. (2003). Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation. Synapse 50, 314–319. Search in Google Scholar

Shen, W., Flajolet, M., Greengard, P., and Surmeier, D.J. (2008). Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848–851. Search in Google Scholar

Shindou, T., Ochi-Shindou, M., and Wickens, J.R. (2011). A Ca(2+) threshold for induction of spike-timing-dependent depression in the mouse striatum. J. Neurosci. 31, 13015–13022. Search in Google Scholar

Singh, V., Carman, M., Roeper, J., and Bonci, A. (2007). Brief ischemia causes long-term depression in midbrain dopamine neurons. Eur. J. Neurosci. 26, 1489–1499. Search in Google Scholar

Smith, Y., Raju, D.V., Pare, J.F., and Sidibe, M. (2004). The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 27, 520–527. Search in Google Scholar

Smith, Y., Galvan, A., Ellender, T.J., Doig, N., Villalba, R.M., Huerta-Ocampo, I., Wichmann, T., and Bolam, J.P. (2014). The thalamostriatal system in normal and diseased states. Front. Syst. Neurosci. 8, 5. Search in Google Scholar

Stefani, A., Peppe, A., Pierantozzi, M., Galati, S., Moschella, V., Stanzione, P., and Mazzone, P. (2009). Multi-target strategy for parkinsonian patients: the role of deep brain stimulation in the centromedian-parafascicularis complex. Brain Res. Bull. 78, 113–118. Search in Google Scholar

Steidl, J.V., Gomez-Isla, T., Mariash, A., Ashe, K.H., and Boland, L.M. (2003). Altered short-term hippocampal synaptic plasticity in mutant alpha-synuclein transgenic mice. NeuroReport 14, 219–223. Search in Google Scholar

Suarez, F., Zhao, Q., Monaghan, D.T., Jane, D.E., Jones, S., and Gibb, A.J. (2010). Functional heterogeneity of NMDA receptors in rat substantia nigra pars compacta and reticulata neurones. Eur. J. Neurosci. 32, 359–367. Search in Google Scholar

Sung, K.W., Choi, S., and Lovinger, D.M. (2001). Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J. Neurophysiol. 86, 2405–2412. Search in Google Scholar

Surmeier, D.J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228–235. Search in Google Scholar

Surmeier, D.J., Plotkin, J., and Shen, W. (2009). Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr. Opin. Neurobiol. 19, 621–628. Search in Google Scholar

Thomas, M.J., Malenka, R.C., and Bonci, A. (2000). Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 20, 5581–5586. Search in Google Scholar

Tigaret, C.M., Thalhammer, A., Rast, G.F., Specht, C.G., Auberson, Y.P., Stewart, M.G., and Schoepfer, R. (2006). Subunit dependencies of N-methyl-D-aspartate (NMDA) receptor-induced alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor internalization. Mol. Pharmacol. 69, 1251–1259. Search in Google Scholar

Tozzi, A., Costa, C., Siliquini, S., Tantucci, M., Picconi, B., Kurz, A., Gispert, S., Auburger, G., and Calabresi, P. (2012). Mechanisms underlying altered striatal synaptic plasticity in old A53T-alpha synuclein overexpressing mice. Neurobiol. Aging 33, 1792–1799. Search in Google Scholar

Tse, Y.C. and Yung, K.K. (2000). Cellular expression of ionotropic glutamate receptor subunits in subpopulations of neurons in the rat substantia nigra pars reticulata. Brain Res. 854, 57–69. Search in Google Scholar

Tseng, K.Y., Riquelme, L.A., Belforte, J.E., Pazo, J.H., and Murer, M.G. (2000). Substantia nigra pars reticulata units in 6-hydroxydopamine-lesioned rats: responses to striatal D2 dopamine receptor stimulation and subthalamic lesions. Eur. J. Neurosci. 12, 247–256. Search in Google Scholar

Tseng, K.Y., Kasanetz, F., Kargieman, L., Pazo, J.H., Murer, M.G., and Riquelme, L.A. (2001). Subthalamic nucleus lesions reduce low frequency oscillatory firing of substantia nigra pars reticulata neurons in a rat model of Parkinson’s disease. Brain Res. 904, 93–103. Search in Google Scholar

Villalba, R.M., Wichmann, T., and Smith, Y. (2014). Neuronal loss in the caudal intralaminar thalamic nuclei in a primate model of Parkinson’s disease. Brain Struct. Funct. 219, 381–394. Search in Google Scholar

Wang, Z., Kai, L., Day, M., Ronesi, J., Yin, H.H., Ding, J., Tkatch, T., Lovinger, D.M., and Surmeier, D.J. (2006). Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50, 443–452. Search in Google Scholar

Watson, J.B., Hatami, A., David, H., Masliah, E., Roberts, K., Evans, C.E., and Levine, M.S. (2009). Alterations in corticostriatal synaptic plasticity in mice overexpressing human alpha-synuclein. Neuroscience 159, 501–513. Search in Google Scholar

Xu, Z., Chen, R.Q., Gu, Q.H., Yan, J.Z., Wang, S.H., Liu, S.Y., and Lu, W. (2009). Metaplastic regulation of long-term potentiation/long-term depression threshold by activity-dependent changes of NR2A/NR2B ratio. J. Neurosci. 29, 8764–8773. Search in Google Scholar

Yamawaki, N., Magill, P.J., Woodhall, G.L., Hall, S.D., and Stanford, I.M. (2012). Frequency selectivity and dopamine-dependence of plasticity at glutamatergic synapses in the subthalamic nucleus. Neuroscience 203, 1–11. Search in Google Scholar

Yashiro, K. and Philpot, B.D. (2008). Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55, 1081–1094. Search in Google Scholar

Yin, H.H. and Lovinger, D.M. (2006). Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. Proc. Natl. Acad. Sci. USA 103, 8251–8256. Search in Google Scholar

Zhang, L.I., Tao, H.W., Holt, C.E., Harris, W.A., and Poo, M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37–44. Search in Google Scholar

Zhou, F.W., Jin, Y., Matta, S.G., Xu, M., and Zhou, F.M. (2009). An ultra-short dopamine pathway regulates basal ganglia output. J. Neurosci. 29, 10424–10435. Search in Google Scholar

Zweifel, L.S., Parker, J.G., Lobb, C.J., Rainwater, A., Wall, V.Z., Fadok, J.P., Darvas, M., Kim, M.J., Mizumori, S.J., Paladini, C.A., et al. (2009). Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. USA 106, 7281–7288. Search in Google Scholar

Received: 2014-3-14
Accepted: 2014-6-20
Published Online: 2014-7-19
Published in Print: 2014-12-1

©2014 by De Gruyter