Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity

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]  E. Richfield,et al.  Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system , 1989, Neuroscience.

[2]  C. Gerfen,et al.  D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. , 1990, Science.

[3]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[4]  F. Gonon.  Prolonged and Extrasynaptic Excitatory Action of Dopamine Mediated by D1 Receptors in the Rat Striatum In Vivo , 1997, The Journal of Neuroscience.

[5]  W. Schultz.  Predictive reward signal of dopamine neurons. , 1998, Journal of neurophysiology.

[6]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[7]  J. Bolam,et al.  Synaptic organisation of the basal ganglia , 2000, Journal of anatomy.

[8]  J. Wickens,et al.  A cellular mechanism of reward-related learning , 2001, Nature.

[9]  D. Lovinger,et al.  Postsynaptic endocannabinoid release is critical to long-term depression in the striatum , 2002, Nature Neuroscience.

[10]  Charles J. Wilson,et al.  Move to the rhythm: oscillations in the subthalamic nucleus–external globus pallidus network , 2002, Trends in Neurosciences.

[11]  K. Dujardin,et al.  Dysfunction of the human memory systems: role of the dopaminergic transmission , 2003, Current opinion in neurology.

[12]  Jonathan D. Cohen,et al.  Computational roles for dopamine in behavioural control , 2004, Nature.

[13]  J. Glowinski,et al.  Bidirectional Activity-Dependent Plasticity at Corticostriatal Synapses , 2005, The Journal of Neuroscience.

[14]  F. Gonon,et al.  Cortical Inputs and GABA Interneurons Imbalance Projection Neurons in the Striatum of Parkinsonian Rats , 2006, The Journal of Neuroscience.

[15]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[16]  K. Fuxe,et al.  Targeting adenosine A2A receptors in Parkinson's disease , 2006, Trends in Neurosciences.

[17]  Kae Nakamura,et al.  Role of Dopamine in the Primate Caudate Nucleus in Reward Modulation of Saccades , 2006, The Journal of Neuroscience.

[18]  Henry H. Yin,et al.  Dopaminergic Control of Corticostriatal Long-Term Synaptic Depression in Medium Spiny Neurons Is Mediated by Cholinergic Interneurons , 2006, Neuron.

[19]  B. Sakmann,et al.  Spine Ca2+ Signaling in Spike-Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[20]  A. Sampson,et al.  Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models , 2006, Nature Neuroscience.

[21]  Robert C. Malenka,et al.  Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models , 2007, Nature.

[22]  D. Lovinger,et al.  Combined Activation of L-Type Ca2+ Channels and Synaptic Transmission Is Sufficient to Induce Striatal Long-Term Depression , 2007, The Journal of Neuroscience.

[23]  D. Surmeier,et al.  D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons , 2007, Trends in Neurosciences.

[24]  Paolo Calabresi,et al.  Dopamine-mediated regulation of corticostriatal synaptic plasticity , 2007, Trends in Neurosciences.

[25]  D. Surmeier,et al.  Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons , 2007, Nature Neuroscience.

[26]  A. Kirkwood,et al.  Neuromodulators Control the Polarity of Spike-Timing-Dependent Synaptic Plasticity , 2007, Neuron.

[27]  L. Trussell,et al.  Coactivation of Pre- and Postsynaptic Signaling Mechanisms Determines Cell-Specific Spike-Timing-Dependent Plasticity , 2007, Neuron.

[28]  P. J. Sjöström,et al.  Dendritic excitability and synaptic plasticity. , 2008, Physiological reviews.

[29]  J. Kerr,et al.  Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.