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

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, 764–773.10.1101/lm.023432.111Search 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, 2403–2409.10.1523/JNEUROSCI.2916-06.2007Search 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, 20564–20569.10.1073/pnas.0706873104Search 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, 6781–6787.10.1523/JNEUROSCI.0280-07.2007Search in Google Scholar

Albin, R.L. (1995). The pathophysiology of chorea/ballism and Parkinsonism. Parkinsonism Relat. Disord. 1, 3–11.10.1016/1353-8020(95)00011-TSearch 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, 266–271.10.1016/0166-2236(90)90107-LSearch 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, 357–381.10.1146/annurev.ne.09.030186.002041Search in Google Scholar PubMed

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, 278–286.10.1038/jcbfm.2012.167Search in Google Scholar PubMed PubMed Central

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, 8272–8281.10.1523/JNEUROSCI.1475-05.2005Search in Google Scholar PubMed PubMed Central

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, 540–548.10.1038/nn.3652Search in Google Scholar PubMed PubMed Central

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, 12513–12522.10.1523/JNEUROSCI.2236-11.2011Search 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, 8161–8165.10.1523/JNEUROSCI.1554-07.2007Search 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, 7410–7419.10.1523/JNEUROSCI.1691-04.2004Search 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, 60–70.10.1016/j.neuropharm.2006.07.013Search 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, 1046–1052.10.1046/j.1460-9568.2003.02543.xSearch 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, 382–389.10.1111/j.1460-9568.1993.tb00505.xSearch in Google Scholar

Bergman, H., Wichmann, T., and DeLong, M.R. (1990). Reversal of experimental Parkinsonism by lesions of the subthalamic nucleus. Science 249, 1436–1438.10.1126/science.2402638Search 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, 507–520.10.1152/jn.1994.72.2.507Search 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, 15531–15541.10.1523/JNEUROSCI.2961-09.2009Search in Google Scholar

Bonifati, V. (2007). Genetics of Parkinsonism. Parkinsonism Relat. Disord. 13(suppl 3), S233–S241.10.1016/S1353-8020(08)70008-7Search 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, 6258–6263.10.1523/JNEUROSCI.1678-08.2008Search 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, 153–166.10.1016/j.neuron.2013.04.039Search 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, 7869–7880.10.1523/JNEUROSCI.0943-12.2012Search 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, 95–99.10.1016/0304-3940(92)90628-KSearch 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, 929–935.10.1111/j.1460-9568.1992.tb00119.xSearch in Google Scholar PubMed

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, 4224–4233.10.1523/JNEUROSCI.12-11-04224.1992Search 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, 4536–4544.10.1523/JNEUROSCI.17-12-04536.1997Search 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, 2489–2499.10.1523/JNEUROSCI.19-07-02489.1999Search in Google Scholar

Calabresi, P., Picconi, B., Tozzi, A., and Di Filippo, M. (2007). Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci. 30, 211–219.10.1016/j.tins.2007.03.001Search in Google Scholar PubMed

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, 8506–8512.10.1523/JNEUROSCI.23-24-08506.2003Search 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, 7036–7040.10.1073/pnas.94.13.7036Search in Google Scholar

Chevalier, G. and Deniau, J.M. (1990). Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277–280.10.1016/0166-2236(90)90109-NSearch 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, 8613–8620.10.1523/JNEUROSCI.17-21-08613.1997Search 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, 2665–2670.10.1073/pnas.94.6.2665Search 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, 190–199.10.1016/j.nbd.2014.04.021Search 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, 238–242.10.1038/nature11846Search 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, 6.10.3389/fnsys.2011.00006Search in Google Scholar

DeLong, M.R. (1990). Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281–285.10.1016/0166-2236(90)90110-VSearch 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, 151–172.10.1016/S0079-6123(06)60009-5Search 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, 294–307.10.1016/j.neuron.2010.06.017Search in Google Scholar PubMed PubMed Central

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, 14331–14341.10.1523/JNEUROSCI.1681-13.2013Search in Google Scholar PubMed PubMed Central

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, 257–272.10.1113/jphysiol.2012.245233Search in Google Scholar PubMed PubMed Central

Fino, E., Glowinski, J., and Venance, L. (2005). Bidirectional activity-dependent plasticity at corticostriatal synapses. J. Neurosci. 25, 11279–11287.10.1523/JNEUROSCI.4476-05.2005Search in Google Scholar PubMed PubMed Central

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, 669–677.10.1523/JNEUROSCI.3921-08.2009Search in Google Scholar PubMed PubMed Central

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, 446–451.10.1038/nn832Search in Google Scholar PubMed

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, 1429–1432.10.1126/science.2147780Search in Google Scholar PubMed

Gertler, T.S., Chan, C.S., and Surmeier, D.J. (2008). Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 28, 10814–10824.10.1523/JNEUROSCI.2660-08.2008Search in Google Scholar PubMed PubMed Central

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, 858–868.10.1016/j.neuron.2011.06.035Search in Google Scholar PubMed PubMed Central

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, 358–363.10.1038/7268Search in Google Scholar PubMed

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, 489–496.10.1016/j.neuron.2005.01.041Search in Google Scholar PubMed

Graybiel, A.M. (2005). The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 15, 638–644.10.1016/j.conb.2005.10.006Search 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, 839–846.10.1016/S0028-3908(01)00021-1Search 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, 13–22.10.1007/s00702-008-0149-xSearch in Google Scholar PubMed

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, 69–74.10.1016/j.brainresbull.2008.09.013Search in Google Scholar PubMed PubMed Central

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, 826–838.10.1016/j.neuron.2009.05.011Search in Google Scholar PubMed PubMed Central

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), 1410–1421.10.1093/brain/123.7.1410Search in Google Scholar PubMed

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, 622–628.10.1002/ana.410440407Search in Google Scholar PubMed

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, 1800–1811.10.1152/jn.01074.2005Search in Google Scholar PubMed

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, 102–106.10.1016/j.neulet.2011.09.007Search in Google Scholar PubMed PubMed Central

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, 9919–9928.10.1523/JNEUROSCI.1404-10.2010Search in Google Scholar PubMed PubMed Central

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, 12115–12124.10.1523/JNEUROSCI.3343-09.2009Search 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, 11441–11446.10.1073/pnas.0702717104Search 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, 613–621.10.1111/j.1471-4159.2009.06152.xSearch 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, 652–662.10.1016/S1474-4422(07)70174-6Search 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, 126–132.10.1523/JNEUROSCI.4287-10.2011Search in Google Scholar PubMed PubMed Central

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, 622–626.10.1038/nature09159Search in Google Scholar PubMed PubMed Central

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, 10537–10545.10.1523/JNEUROSCI.2959-05.2005Search in Google Scholar PubMed PubMed Central

Kreitzer, A.C. and Malenka, R.C. (2007). Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature 445, 643–647.10.1038/nature05506Search in Google Scholar PubMed

Kreitzer, A.C. and Malenka, R.C. (2008). Striatal plasticity and basal ganglia circuit function. Neuron 60, 543–554.10.1016/j.neuron.2008.11.005Search in Google Scholar PubMed PubMed Central

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, 7931–7940.10.1523/JNEUROSCI.22-18-07931.2002Search in Google Scholar

Lerner, T.N. and Kreitzer, A.C. (2011). Neuromodulatory control of striatal plasticity and behavior. Curr. Opin. Neurobiol. 21, 322–327.10.1016/j.conb.2011.01.005Search 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, 347–359.10.1016/j.neuron.2011.11.015Search 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, 2160–2164.10.1523/JNEUROSCI.5844-09.2010Search 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, 7766–7775.10.1523/JNEUROSCI.20-20-07766.2000Search 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, 1788–1797.10.1523/JNEUROSCI.5604-09.2010Search 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, 91–95.10.1016/S0140-6736(95)90062-4Search 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, 359–374.10.1093/brain/awq332Search in Google Scholar PubMed

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, 1021–1024.10.1126/science.1096615Search in Google Scholar PubMed

Luscher, C. and Malenka, R.C. (2011). Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650–663.10.1016/j.neuron.2011.01.017Search in Google Scholar PubMed PubMed Central

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, 126–135.10.1016/j.neuroscience.2011.07.065Search in Google Scholar PubMed

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, 700–714.10.1152/jn.00134.2004Search in Google Scholar PubMed

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, 3875–3884.10.1523/JNEUROSCI.4439-05.2006Search in Google Scholar PubMed PubMed Central

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, 14245–14258.10.1523/JNEUROSCI.4199-08.2008Search in Google Scholar PubMed PubMed Central

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, 4795–4806.10.1523/JNEUROSCI.0123-08.2008Search in Google Scholar PubMed PubMed Central

Mathur, B.N. and Lovinger, D.M. (2012). Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front. Pharmacol. 3, 66.10.3389/fphar.2012.00066Search in Google Scholar PubMed PubMed Central

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, 960–976.10.1152/jn.2001.85.2.960Search in Google Scholar PubMed

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, 9539–9546.10.1523/JNEUROSCI.18-22-09539.1998Search 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, 221–228.10.1111/j.1525-1403.2006.00063.xSearch in Google Scholar PubMed

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, 503–517.10.1016/j.nbd.2010.07.010Search in Google Scholar PubMed PubMed Central

Minamimoto, T., Hori, Y., and Kimura, M. (2005). Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308, 1798–1801.10.1126/science.1109154Search in Google Scholar PubMed

Missale, C., Nash, S.R., Robinson, S.W., Jaber, M., and Caron, M.G. (1998). Dopamine receptors: from structure to function. Physiol. Rev. 78, 189–225.10.1152/physrev.1998.78.1.189Search in Google Scholar

Montague, P.R., Hyman, S.E., and Cohen, J.D. (2004). Computational roles for dopamine in behavioural control. Nature 431, 760–767.10.1038/nature03015Search 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, 395–405.10.1101/lm.1398709Search 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, 278–293.10.1002/(SICI)1098-2396(199712)27:4<278::AID-SYN2>3.0.CO;2-9Search 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, 2671–2683.10.1523/JNEUROSCI.16-08-02671.1996Search 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, 588–598.10.1111/j.1460-9568.2008.06598.xSearch 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, 284–293.10.1038/nn.3022Search 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–S19.10.1016/S1471-1931(00)00028-8Search 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, 150–159.10.1016/S0006-8993(98)01049-XSearch 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, 433–442.10.1016/S0006-8993(99)01121-XSearch 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, 221–226.10.1097/00001756-199902050-00004Search in Google Scholar PubMed

Packard, M.G. and Knowlton, B.J. (2002). Learning and memory functions of the basal ganglia. Annu. Rev. Neurosci. 25, 563–593.10.1146/annurev.neuro.25.112701.142937Search in Google Scholar PubMed

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, 14182–14193.10.1523/JNEUROSCI.2149-10.2010Search in Google Scholar PubMed PubMed Central

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, 9353–9363.10.1523/JNEUROSCI.5796-12.2013Search in Google Scholar PubMed PubMed Central

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, 2635–2645.10.1093/brain/awf269Search in Google Scholar PubMed

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, 501–506.10.1038/nn1040Search in Google Scholar PubMed

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, 1661–1669.10.1093/brain/awh190Search in Google Scholar PubMed

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, 309–318.10.1093/brain/awn322Search in Google Scholar PubMed

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, 379–390.10.1016/j.nbd.2012.06.009Search in Google Scholar PubMed

Radnikow, G. and Misgeld, U. (1998). Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J. Neurosci. 18, 2009–2016.10.1523/JNEUROSCI.18-06-02009.1998Search 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, RC128.10.1523/JNEUROSCI.21-03-j0006.2001Search 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, 199–203.10.1016/S0306-4522(00)00273-6Search 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, 204–208.10.1016/0304-3940(88)90382-5Search 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, 3326–3331.10.1523/JNEUROSCI.09-09-03326.1989Search 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, 245–256.10.1113/jphysiol.2004.068460Search in Google Scholar PubMed PubMed Central

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, 1673–1679.10.1523/JNEUROSCI.5214-03.2004Search in Google Scholar PubMed PubMed Central

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, 7583–7594.10.1523/JNEUROSCI.4932-12.2013Search in Google Scholar PubMed PubMed Central

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, 1118–1124.10.1038/nn.3456Search in Google Scholar PubMed PubMed Central

Schultz, W. (1998). Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1–27.10.1152/jn.1998.80.1.1Search in Google Scholar PubMed

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), 331–341.10.1111/j.1469-7793.2000.00331.xSearch in Google Scholar PubMed PubMed Central

Shen, K.Z. and Johnson, S.W. (2001). Presynaptic GABA(B) receptors inhibit synaptic inputs to rat subthalamic neurons. Neuroscience 108, 431–436.10.1016/S0306-4522(01)00424-9Search 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, 219–230.10.1113/jphysiol.2001.013404Search 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, 489–496.10.1113/jphysiol.2003.052209Search 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, 99–106.10.1016/S0306-4522(02)00656-5Search 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, 1029–1033.10.1016/j.neuroscience.2007.12.001Search in Google Scholar PubMed PubMed Central

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, 314–319.10.1002/syn.10274Search in Google Scholar PubMed

Shen, W., Flajolet, M., Greengard, P., and Surmeier, D.J. (2008). Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848–851.10.1126/science.1160575Search in Google Scholar PubMed PubMed Central

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, 13015–13022.10.1523/JNEUROSCI.3206-11.2011Search in Google Scholar PubMed PubMed Central

Singh, V., Carman, M., Roeper, J., and Bonci, A. (2007). Brief ischemia causes long-term depression in midbrain dopamine neurons. Eur. J. Neurosci. 26, 1489–1499.10.1111/j.1460-9568.2007.05781.xSearch in Google Scholar PubMed

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, 520–527.10.1016/j.tins.2004.07.004Search in Google Scholar PubMed

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, 5.10.3389/fnsys.2014.00005Search in Google Scholar PubMed PubMed Central

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, 113–118.10.1016/j.brainresbull.2008.08.007Search in Google Scholar PubMed

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, 219–223.10.1097/00001756-200302100-00012Search in Google Scholar PubMed

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, 359–367.10.1111/j.1460-9568.2010.07298.xSearch in Google Scholar PubMed PubMed Central

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, 2405–2412.10.1152/jn.2001.86.5.2405Search in Google Scholar PubMed

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, 228–235.10.1016/j.tins.2007.03.008Search in Google Scholar PubMed

Surmeier, D.J., Plotkin, J., and Shen, W. (2009). Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr. Opin. Neurobiol. 19, 621–628.10.1016/j.conb.2009.10.003Search in Google Scholar PubMed PubMed Central

Thomas, M.J., Malenka, R.C., and Bonci, A. (2000). Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci. 20, 5581–5586.10.1523/JNEUROSCI.20-15-05581.2000Search 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, 1251–1259.10.1124/mol.105.018580Search in Google Scholar PubMed

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, 1792–1799.10.1016/j.neurobiolaging.2011.05.002Search in Google Scholar PubMed

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, 57–69.10.1016/S0006-8993(99)02292-1Search 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, 247–256.10.1046/j.1460-9568.2000.00910.xSearch 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, 93–103.10.1016/S0006-8993(01)02489-1Search 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, 381–394.10.1007/s00429-013-0507-9Search in Google Scholar PubMed PubMed Central

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, 443–452.10.1016/j.neuron.2006.04.010Search in Google Scholar PubMed

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, 501–513.10.1016/j.neuroscience.2009.01.021Search in Google Scholar PubMed PubMed Central

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, 8764–8773.10.1523/JNEUROSCI.1014-09.2009Search in Google Scholar PubMed PubMed Central

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, 1–11.10.1016/j.neuroscience.2011.12.027Search in Google Scholar PubMed PubMed Central

Yashiro, K. and Philpot, B.D. (2008). Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 55, 1081–1094.10.1016/j.neuropharm.2008.07.046Search in Google Scholar PubMed PubMed Central

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, 8251–8256.10.1073/pnas.0510797103Search in Google Scholar PubMed PubMed Central

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, 37–44.10.1038/25665Search in Google Scholar PubMed

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, 10424–10435.10.1523/JNEUROSCI.4402-08.2009Search in Google Scholar PubMed PubMed Central

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, 7281–7288.10.1073/pnas.0813415106Search in Google Scholar PubMed PubMed Central