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Science 321 (5890): 848-851

Copyright © 2008 by the American Association for the Advancement of Science

Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity

Weixing Shen,1 Marc Flajolet,2 Paul Greengard,2 D. James Surmeier1*

Abstract: At synapses between cortical pyramidal neurons and principal striatal medium spiny neurons (MSNs), postsynaptic D1 and D2 dopamine (DA) receptors are postulated to be necessary for the induction of long-term potentiation and depression, respectively—forms of plasticity thought to underlie associative learning. Because these receptors are restricted to two distinct MSN populations, this postulate demands that synaptic plasticity be unidirectional in each cell type. Using brain slices from DA receptor transgenic mice, we show that this is not the case. Rather, DA plays complementary roles in these two types of MSN to ensure that synaptic plasticity is bidirectional and Hebbian. In models of Parkinson's disease, this system is thrown out of balance, leading to unidirectional changes in plasticity that could underlie network pathology and symptoms.

1 Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.
2 Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.

* To whom correspondence should be addressed. E-mail: j-surmeier{at}northwestern.edu


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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V. Paille, B. Picconi, V. Bagetta, V. Ghiglieri, C. Sgobio, M. Di Filippo, M. T. Viscomi, C. Giampa, F. R. Fusco, F. Gardoni, et al. (2010)
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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E. Fino, V. Paille, Y. Cui, T. Morera-Herreras, J.-M. Deniau, and L. Venance (2010)
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   Abstract »    Full Text »    PDF »
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A. El Manira and A. Kyriakatos (2010)
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   Abstract »    Full Text »    PDF »
Absence of NMDA receptors in dopamine neurons attenuates dopamine release but not conditioned approach during Pavlovian conditioning.
J. G. Parker, L. S. Zweifel, J. J. Clark, S. B. Evans, P. E. M. Phillips, and R. D. Palmiter (2010)
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   Abstract »    Full Text »    PDF »
Presynaptic dopaminergic compartment determines the susceptibility to L-DOPA-induced dyskinesia in rats.
A. Ulusoy, G. Sahin, and D. Kirik (2010)
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   Abstract »    Full Text »    PDF »
Dopaminergic Modulation of Endocannabinoid-Mediated Plasticity at GABAergic Synapses in the Prefrontal Cortex.
C. Q. Chiu, N. Puente, P. Grandes, and P. E. Castillo (2010)
J. Neurosci. 30, 7236-7248
   Abstract »    Full Text »    PDF »
Dopaminergic Dysfunction in Schizophrenia: Salience Attribution Revisited.
A. Heinz and F. Schlagenhauf (2010)
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   Abstract »    Full Text »    PDF »
Dopamine D2 receptor density in the limbic striatum is related to implicit but not explicit movement sequence learning.
A. Karabanov, S. Cervenka, O. de Manzano, H. Forssberg, L. Farde, and F. Ullen (2010)
PNAS 107, 7574-7579
   Abstract »    Full Text »    PDF »
Changing Views of Basal Ganglia Circuits and Circuit Disorders.
M. DeLong and T. Wichmann (2010)
Clinical EEG and Neuroscience 41, 61-67
   Abstract »    Full Text »    PDF »
Loss of GluN2B-Containing NMDA Receptors in CA1 Hippocampus and Cortex Impairs Long-Term Depression, Reduces Dendritic Spine Density, and Disrupts Learning.
J. L. Brigman, T. Wright, G. Talani, S. Prasad-Mulcare, S. Jinde, G. K. Seabold, P. Mathur, M. I. Davis, R. Bock, R. M. Gustin, et al. (2010)
J. Neurosci. 30, 4590-4600
   Abstract »    Full Text »    PDF »
Endocannabinoid Signaling Mediates Psychomotor Activation by Adenosine A2A Antagonists.
T. N. Lerner, E. A. Horne, N. Stella, and A. C. Kreitzer (2010)
J. Neurosci. 30, 2160-2164
   Abstract »    Full Text »    PDF »
Cellular Mechanisms Underlying Burst Firing in Substantia Nigra Dopamine Neurons.
S. N. Blythe, D. Wokosin, J. F. Atherton, and M. D. Bevan (2009)
J. Neurosci. 29, 15531-15541
   Abstract »    Full Text »    PDF »
Genetic Deletion of A2A Adenosine Receptors in the Striatum Selectively Impairs Habit Formation.
C. Yu, J. Gupta, J.-F. Chen, and H. H. Yin (2009)
J. Neurosci. 29, 15100-15103
   Abstract »    Full Text »    PDF »
Autocrine Activation of Neuronal NMDA Receptors by Aspartate Mediates Dopamine- and cAMP-Induced CREB-Dependent Gene Transcription.
L. E. F. Almeida, P. D. Murray, H. R. Zielke, C. D. Roby, T. J. Kingsbury, and B. K. Krueger (2009)
J. Neurosci. 29, 12702-12710
   Abstract »    Full Text »    PDF »
Do Substantia Nigra Dopaminergic Neurons Differentiate Between Reward and Punishment?.
M. J. Frank and D. J. Surmeier (2009)
J Mol Cell Biol 1, 15-16
   Abstract »    Full Text »    PDF »
Adenylyl Cyclase Type 5 Contributes to Corticostriatal Plasticity and Striatum-Dependent Learning.
M. A. Kheirbek, J. P. Britt, J. A. Beeler, Y. Ishikawa, D. S. McGehee, and X. Zhuang (2009)
J. Neurosci. 29, 12115-12124
   Abstract »    Full Text »    PDF »
Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine.
G. Martella, A. Tassone, G. Sciamanna, P. Platania, D. Cuomo, M. T. Viscomi, P. Bonsi, E. Cacci, S. Biagioni, A. Usiello, et al. (2009)
Brain 132, 2336-2349
   Abstract »    Full Text »    PDF »
Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses.
J.-C. Zhang, P.-M. Lau, and G.-Q. Bi (2009)
PNAS 106, 13028-13033
   Abstract »    Full Text »    PDF »
Diversity in long-term synaptic plasticity at inhibitory synapses of striatal spiny neurons.
P. E. Rueda-Orozco, E. Mendoza, R. Hernandez, J. J. Aceves, O. Ibanez-Sandoval, E. Galarraga, and J. Bargas (2009)
Learn. Mem. 16, 474-478
   Abstract »    Full Text »    PDF »
From Real-World Events to Psychosis: The Emerging Neuropharmacology of Delusions.
P. D. Morrison and R. M. Murray (2009)
Schizophr Bull 35, 668-674
   Abstract »    Full Text »    PDF »
Dopamine Depletion Induces Distinct Compensatory Gene Expression Changes in DARPP-32 Signal Transduction Cascades of Striatonigral and Striatopallidal Neurons.
B. H. Meurers, G. Dziewczapolski, T. Shi, A. Bittner, F. Kamme, and C. W. Shults (2009)
J. Neurosci. 29, 6828-6839
   Abstract »    Full Text »    PDF »
Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning.
H.-C. Tsai, F. Zhang, A. Adamantidis, G. D. Stuber, A. Bonci, L. de Lecea, and K. Deisseroth (2009)
Science 324, 1080-1084
   Abstract »    Full Text »    PDF »
Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior.
L. S. Zweifel, J. G. Parker, C. J. Lobb, A. Rainwater, V. Z. Wall, J. P. Fadok, M. Darvas, M. J. Kim, S. J. Y. Mizumori, C. A. Paladini, et al. (2009)
PNAS 106, 7281-7288
   Abstract »    Full Text »    PDF »
Gap Junctions between Striatal Fast-Spiking Interneurons Regulate Spiking Activity and Synchronization as a Function of Cortical Activity.
J. Hjorth, K. T. Blackwell, and J. Hellgren Kotaleski (2009)
J. Neurosci. 29, 5276-5286
   Abstract »    Full Text »    PDF »
Phosphorylation of Rap1GAP, a striatally enriched protein, by protein kinase A controls Rap1 activity and dendritic spine morphology.
T. McAvoy, M.-m. Zhou, P. Greengard, and A. C. Nairn (2009)
PNAS 106, 3531-3536
   Abstract »    Full Text »    PDF »
A Role for Dopamine in Temporal Decision Making and Reward Maximization in Parkinsonism.
A. A. Moustafa, M. X. Cohen, S. J. Sherman, and M. J. Frank (2008)
J. Neurosci. 28, 12294-12304
   Abstract »    Full Text »    PDF »
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M. J. Frank (2008)
Schizophr Bull 34, 1008-1011
   Full Text »    PDF »
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J. Moss and J. P. Bolam (2008)
J. Neurosci. 28, 11221-11230
   Abstract »    Full Text »    PDF »
Dopamine D1 receptor inhibition of NMDA receptor currents mediated by tyrosine kinase-dependent receptor trafficking in neonatal rat striatum.
H. Tong and A. J. Gibb (2008)
J. Physiol. 586, 4693-4707
   Abstract »    Full Text »    PDF »

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