Dopaminergic modulation of striatal neurons, circuits, and assemblies

In recent years, there has been a great deal of progress toward understanding the role of the striatum and dopamine in action selection. The advent of new animal models and the development of optical techniques for imaging and stimulating select neuronal populations have provided the means by which identified synapses, cells, and circuits can be reliably studied. This review attempts to summarize some of the key advances in this broad area, focusing on dopaminergic modulation of intrinsic excitability and synaptic plasticity in canonical microcircuits in the striatum as well as recent work suggesting that there are neuronal assemblies within the striatum devoted to particular types of computation and possibly action selection.

[1]  Shiaoching Gong,et al.  A gene expression atlas of the central nervous system based on bacterial artificial chromosomes , 2003, Nature.

[2]  P. Ekman.  Facial expressions of emotion: an old controversy and new findings. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  G. Edelman,et al.  Theoretical neuroanatomy and the connectivity of the cerebral cortex , 2002, Behavioural Brain Research.

[4]  Jérôme Baufreton,et al.  Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. , 2009, Journal of neurophysiology.

[5]  Charles J. Wilson,et al.  Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. , 1994, Journal of neurophysiology.

[6]  Bernardo L Sabatini,et al.  Timing and Location of Synaptic Inputs Determine Modes of Subthreshold Integration in Striatal Medium Spiny Neurons , 2007, The Journal of Neuroscience.

[7]  D. Plenz,et al.  Action Potential Timing Determines Dendritic Calcium during Striatal Up-States , 2004, The Journal of Neuroscience.

[8]  Barbara Hammer,et al.  Compositionality in Neural Systems , 2002 .

[9]  J. Bargas,et al.  Spontaneous Voltage Oscillations in Striatal Projection Neurons in a Rat Corticostriatal Slice , 2003, The Journal of physiology.

[10]  Luis Carrillo-Reid,et al.  Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses , 2007, Proceedings of the National Academy of Sciences.

[11]  M. Wolf,et al.  Dopamine Receptor Stimulation Modulates AMPA Receptor Synaptic Insertion in Prefrontal Cortex Neurons , 2005, The Journal of Neuroscience.

[12]  D. Surmeier,et al.  Neuromodulation of Na+ Channel Slow Inactivation via cAMP-Dependent Protein Kinase and Protein Kinase C , 2006, Neuron.

[13]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[14]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  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.

[16]  J. Bargas,et al.  Dynamics of the Parkinsonian Striatal Microcircuit: Entrainment into a Dominant Network State , 2010, The Journal of Neuroscience.

[17]  D. Standaert,et al.  Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  Alexander B. Wiltschko,et al.  Selective Activation of Striatal Fast-Spiking Interneurons during Choice Execution , 2010, Neuron.

[19]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[20]  M. Delong,et al.  Functional neuroanatomy of the basal ganglia in Parkinson's disease. , 2003, Advances in neurology.

[21]  H. Markram,et al.  Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat , 2004, The Journal of physiology.

[22]  D. Lovinger,et al.  Short- and long-term synaptic depression in rat neostriatum. , 1993, Journal of neurophysiology.

[23]  Enrico Bracci,et al.  Dopamine excites fast-spiking interneurons in the striatum. , 2002, Journal of neurophysiology.

[24]  G. Lynch,et al.  Presynaptic BDNF Promotes Postsynaptic Long-Term Potentiation in the Dorsal Striatum , 2010, The Journal of Neuroscience.

[25]  Kitai St,et al.  Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons. , 1993 .

[26]  D. Surmeier,et al.  Dopamine receptor subtypes colocalize in rat striatonigral neurons. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Charles J. Wilson,et al.  RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion , 2006, Nature Neuroscience.

[28]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

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

[30]  J. Csicsvari,et al.  Organization of cell assemblies in the hippocampus , 2003, Nature.

[31]  Y. Kawaguchi,et al.  Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  C. Gerfen,et al.  Modulation of striatal projection systems by dopamine. , 2011, Annual review of neuroscience.

[33]  Bruce L McNaughton,et al.  Cannabinoids reveal importance of spike timing coordination in hippocampal function , 2006, Nature Neuroscience.

[34]  H. Kita,et al.  Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study , 1990, Brain Research.

[35]  Charles J. Wilson,et al.  Comparison of IPSCs Evoked by Spiny and Fast-Spiking Neurons in the Neostriatum , 2004, The Journal of Neuroscience.

[36]  C. Stevens,et al.  Synaptic noise and other sources of randomness in motoneuron interspike intervals. , 1968, Journal of neurophysiology.

[37]  D. James Surmeier,et al.  Re-emergence of striatal cholinergic interneurons in movement disorders , 2007, Trends in Neurosciences.

[38]  Amiram Grinvald,et al.  Imaging input and output dynamics of neocortical networks in vivo: exciting times ahead. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Maloteaux,et al.  Altered expression of regulators of G-protein signaling (RGS) mRNAs in the striatum of rats undergoing dopamine depletion. , 2003, Biochemical pharmacology.

[40]  K. Harris.  Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[41]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[42]  P. Calabresi,et al.  Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: Evidence for D1 receptor involvement , 1987, Neuroscience.

[43]  T E Salt,et al.  Effects of excitatory amino acids and their antagonists on membrane and action potentials of cat caudate neurones. , 1983, The Journal of physiology.

[44]  Angus C. Nairn,et al.  Synaptic plasticity: one STEP at a time , 2006, Trends in Neurosciences.

[45]  Laurent Venance,et al.  Spike-timing dependent plasticity in striatal interneurons , 2011, Neuropharmacology.

[46]  D. Surmeier,et al.  D5 Dopamine Receptors Enhance Zn2+-Sensitive GABAA Currents in Striatal Cholinergic Interneurons through a PKA/PP1 Cascade , 1997, Neuron.

[47]  S. Green,et al.  cAMP-Dependent Regulation of Cardiac L-Type Ca2+ Channels Requires Membrane Targeting of PKA and Phosphorylation of Channel Subunits , 1997, Neuron.

[48]  Luis Carrillo-Reid,et al.  Activation of the cholinergic system endows compositional properties to striatal cell assemblies. , 2009, Journal of neurophysiology.

[49]  Alexander B. Wiltschko,et al.  Opposite Effects of Stimulant and Antipsychotic Drugs on Striatal Fast-Spiking Interneurons , 2010, Neuropsychopharmacology.

[50]  J. Dostrovsky,et al.  Neuronal Oscillations in the Basal Ganglia and Movement Disorders: Evidence from Whole Animal and Human Recordings , 2004, The Journal of Neuroscience.

[51]  Yuji Ikegaya,et al.  Scale-free topology of the CA3 hippocampal network: a novel method to analyze functional neuronal assemblies. , 2010, Biophysical journal.

[52]  E. Callaway,et al.  Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity , 2005, Nature Neuroscience.

[53]  J. C. Stoof,et al.  Two dopamine receptors: biochemistry, physiology and pharmacology. , 1984, Life sciences.

[54]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[55]  K. Fuxe,et al.  Adenosine receptor–dopamine receptor interactions in the basal ganglia and their relevance for brain function , 2007, Physiology & Behavior.

[56]  Charles J. Wilson,et al.  Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons , 2008, Brain Research Reviews.

[57]  Rhea R. Kimpo,et al.  Cellular, Circuit, and Synaptic Mechanisms in Song Learning , 2004, Annals of the New York Academy of Sciences.

[58]  C. Cepeda,et al.  Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Anatol C. Kreitzer,et al.  Dopamine Modulation of State-Dependent Endocannabinoid Release and Long-Term Depression in the Striatum , 2005, The Journal of Neuroscience.

[60]  C. Stoetzner,et al.  State-dependent plasticity of the corticostriatal pathway , 2010, Neuroscience.

[61]  Henrike Planert,et al.  Dynamics of Synaptic Transmission between Fast-Spiking Interneurons and Striatal Projection Neurons of the Direct and Indirect Pathways , 2010, The Journal of Neuroscience.

[62]  J. Bolam,et al.  Selective Innervation of Neostriatal Interneurons by a Subclass of Neuron in the Globus Pallidus of the Rat , 1998, The Journal of Neuroscience.

[63]  J. Bolam,et al.  Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  T. Brown.  The intrinsic factors in the act of progression in the mammal , 1911 .

[65]  J. Bargas,et al.  Dopaminergic Modulation of Axon Collaterals Interconnecting Spiny Neurons of the Rat Striatum , 2003, The Journal of Neuroscience.

[66]  D. Plenz,et al.  Dendritic Calcium Encodes Striatal Neuron Output during Up-States , 2002, The Journal of Neuroscience.

[67]  C. Cepeda,et al.  Modulation of AMPA currents by D2 dopamine receptors in striatal medium‐sized spiny neurons: are dendrites necessary? , 2004, The European journal of neuroscience.

[68]  P. Somogyi,et al.  Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study , 1983, Journal of neurocytology.

[69]  J. Marshall,et al.  Molecular, chemical, and anatomical characterization of globus pallidus dopamine D2 receptor mRNA‐containing neurons , 2004, Synapse.

[70]  Henry A. Lester,et al.  Chronic Nicotine Selectively Enhances α4β2* Nicotinic Acetylcholine Receptors in the Nigrostriatal Dopamine Pathway , 2009, The Journal of Neuroscience.

[71]  Mary Kay Lobo,et al.  FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains , 2006, Nature Neuroscience.

[72]  B. D. Bennett,et al.  Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat , 1994, Neuroscience.

[73]  S. Charpier,et al.  In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex , 1999, Neuroscience.

[74]  D. Lovinger,et al.  Frequency-Dependent Inversion of Net Striatal Output by Endocannabinoid-Dependent Plasticity at Different Synaptic Inputs , 2009, The Journal of Neuroscience.

[75]  D. Surmeier,et al.  Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. , 1998, Advances in pharmacology.

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

[77]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[78]  J. Bargas,et al.  Passive properties of neostriatal neurons during potassium conductance blockade , 1998, Experimental Brain Research.

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

[80]  T. Scheuer,et al.  Control of neuronal excitability by phosphorylation and dephosphorylation of sodium channels. , 2006, Biochemical Society transactions.

[81]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[82]  R. Huganir,et al.  Alterations in subunit expression, composition, and phosphorylation of striatal N-methyl-D-aspartate glutamate receptors in a rat 6-hydroxydopamine model of Parkinson's disease. , 2000, Molecular pharmacology.

[83]  J. Bargas,et al.  Dopamine selects glutamatergic inputs to neostriatal neurons , 1997, Synapse.

[84]  J. Hounsgaard,et al.  NMDA-Induced intrinsic voltage oscillations depend on L-type calcium channels in spinal motoneurons of adult turtles. , 1998, Journal of neurophysiology.

[85]  C.J. Wilson,et al.  Understanding the neostriatal microcircuitry: High‐voltage electron microscopy , 1994, Microscopy research and technique.

[86]  Ad Aertsen,et al.  Synaptic integration in rat frontal cortex shaped by network activity. , 2005, Journal of neurophysiology.

[87]  A. Grinvald,et al.  Neuronal assemblies: Single cortical neurons are obedient members of a huge orchestra , 2003, Biopolymers.

[88]  P. Greengard,et al.  A Translational Profiling Approach for the Molecular Characterization of CNS Cell Types , 2008, Cell.

[89]  J. Lübke,et al.  Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats , 2006, The Journal of physiology.

[90]  J. Tepper,et al.  Heterogeneity and Diversity of Striatal GABAergic Interneurons , 2010, Front. Neuroanat..

[91]  P. Greengard,et al.  Regulation of Phosphorylation of the GluR1 AMPA Receptor in the Neostriatum by Dopamine and Psychostimulants In Vivo , 2000, The Journal of Neuroscience.

[92]  J. Bargas,et al.  Ca2+ channels that activate Ca2+-dependent K+ currents in neostriatal neurons , 1999, Neuroscience.

[93]  A. Bittner,et al.  Dopamine Depletion Induces Distinct Compensatory Gene Expression Changes in DARPP-32 Signal Transduction Cascades of Striatonigral and Striatopallidal Neurons , 2009, The Journal of Neuroscience.

[94]  S. Grillner,et al.  Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. , 1981, Acta physiologica Scandinavica.

[95]  J. Tepper,et al.  Dual Cholinergic Control of Fast-Spiking Interneurons in the Neostriatum , 2002, The Journal of Neuroscience.

[96]  A M Graybiel,et al.  Cortically Driven Immediate-Early Gene Expression Reflects Modular Influence of Sensorimotor Cortex on Identified Striatal Neurons in the Squirrel Monkey , 1997, The Journal of Neuroscience.

[97]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[98]  Enrico Bracci,et al.  Activation of dopamine D1‐like receptors excites LTS interneurons of the striatum , 2002, The European journal of neuroscience.

[99]  Antonio Pisani,et al.  Receptor Subtypes Involved in the Presynaptic and Postsynaptic Actions of Dopamine on Striatal Interneurons , 2003, The Journal of Neuroscience.

[100]  J. Bargas,et al.  Dopamine facilitates striatal EPSPs through an L‐type Ca2+ conductance , 1997, Neuroreport.

[101]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[102]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[103]  Joshua L Plotkin,et al.  Differential Excitability and Modulation of Striatal Medium Spiny Neuron Dendrites , 2008, The Journal of Neuroscience.

[104]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[105]  D. Lovinger,et al.  Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[106]  J. Bargas,et al.  D1 Receptor Activation Enhances Evoked Discharge in Neostriatal Medium Spiny Neurons by Modulating an L-Type Ca2+ Conductance , 1997, The Journal of Neuroscience.

[107]  Charles J. Wilson,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase , 1980 .

[108]  H. Kita,et al.  GABAergic circuits of the striatum. , 1993, Progress in brain research.

[109]  C. Cepeda,et al.  Calcium modulates dopamine potentiation of N‐methyl‐D‐aspartate Responses: Electrophysiological and imaging evidence , 2004, Journal of neuroscience research.

[110]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[111]  B. Sabatini,et al.  State-Dependent Calcium Signaling in Dendritic Spines of Striatal Medium Spiny Neurons , 2004, Neuron.

[112]  D. Surmeier,et al.  Dichotomous Anatomical Properties of Adult Striatal Medium Spiny Neurons , 2008, The Journal of Neuroscience.

[113]  Charles J. Wilson.  Dendritic morphology, inward rectification, and the functional properties of neostriatal neurons , 1992 .

[114]  Bernardo L. Sabatini,et al.  Competitive regulation of synaptic Ca influx by D2 dopamine and A2A adenosine receptors , 2010, Nature Neuroscience.

[115]  Luis Carrillo-Reid,et al.  Encoding network states by striatal cell assemblies. , 2008, Journal of neurophysiology.

[116]  William A Catterall,et al.  Transmitter Modulation of Slow, Activity-Dependent Alterations in Sodium Channel Availability Endows Neurons with a Novel Form of Cellular Plasticity , 2003, Neuron.

[117]  P. Greengard,et al.  Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity , 2008, Science.

[118]  D. James Surmeier,et al.  G-Protein-Coupled Receptor Modulation of Striatal CaV1.3 L-Type Ca Channels Is Dependent on a Shank-Binding Domain , 2005 .

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

[120]  Hui Zhang,et al.  Heterosynaptic Dopamine Neurotransmission Selects Sets of Corticostriatal Terminals , 2004, Neuron.

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

[122]  J. Houk,et al.  Network models of the basal ganglia , 1997, Current Opinion in Neurobiology.

[123]  M. Steriade.  Coherent oscillations and short-term plasticity in corticothalamic networks , 1999, Trends in Neurosciences.

[124]  J. Obeso,et al.  Functional organization of the basal ganglia: Therapeutic implications for Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[125]  N. Rajakumar,et al.  The pallidostriatal projection in the rat: a recurrent inhibitory loop? , 1994, Brain Research.

[126]  P. Greengard,et al.  The phosphoprotein DARPP-32 mediates cAMP-dependent potentiation of striatal N-methyl-D-aspartate responses. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[127]  P. Greengard,et al.  Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines , 2006, European Neuropsychopharmacology.

[128]  P. Groves,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. , 1980, The Journal of comparative neurology.

[129]  S. Charpier,et al.  In vivo activity-dependent plasticity at cortico-striatal connections: evidence for physiological long-term potentiation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[131]  P. Groves.  A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement , 1983, Brain Research Reviews.

[132]  Dietmar Plenz,et al.  Fast synaptic transmission between striatal spiny projection neurons , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[133]  Dagoberto Tapia,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[134]  Huanmian Chen,et al.  Recurrent Inhibitory Network among Striatal Cholinergic Interneurons , 2008, The Journal of Neuroscience.

[135]  K Ossowska,et al.  Stimulation of glutamate receptors in the intermediate/caudal striatum induces contralateral turning. , 1995, European journal of pharmacology.

[136]  D. Surmeier,et al.  Muscarinic (m2/m4) receptors reduce N- and P-type Ca2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane- delimited, G-protein pathway , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[137]  G. Fisone,et al.  Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice , 2009, Trends in Neurosciences.

[138]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[139]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[140]  David G Standaert,et al.  Dopamine D1 Activation Potentiates Striatal NMDA Receptors by Tyrosine Phosphorylation-Dependent Subunit Trafficking , 2006, The Journal of Neuroscience.

[141]  Elvira Galarraga,et al.  Diversity in long-term synaptic plasticity at inhibitory synapses of striatal spiny neurons. , 2009, Learning & memory.

[142]  Charles J. Wilson,et al.  The generation of natural firing patterns in neostriatal neurons. , 1993, Progress in brain research.

[143]  J. Surmeier,et al.  D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. , 1997, Journal of neurophysiology.

[144]  J. Berke,et al.  Fast oscillations in cortical‐striatal networks switch frequency following rewarding events and stimulant drugs , 2009, The European journal of neuroscience.

[145]  Jean-Pierre Rospars,et al.  REVIEW ARTICLE: Neuronal coding and spiking randomness , 2007, The European journal of neuroscience.

[146]  D. James Surmeier,et al.  Thalamic Gating of Corticostriatal Signaling by Cholinergic Interneurons , 2010, Neuron.

[147]  Garrett E. Alexander.  Basal ganglia , 1998 .

[148]  Nicolas Maurice,et al.  D2 Dopamine Receptor-Mediated Modulation of Voltage-Dependent Na+ Channels Reduces Autonomous Activity in Striatal Cholinergic Interneurons , 2004, The Journal of Neuroscience.

[149]  Joel L. Davis,et al.  Single neuron computation , 1992 .

[150]  Anatol C. Kreitzer,et al.  Cholinergic Interneurons Mediate Fast VGluT3-Dependent Glutamatergic Transmission in the Striatum , 2011, PloS one.

[151]  S. Haber,et al.  Ventral pallidostriatal pathway in the monkey: Evidence for modulation of basal ganglia circuits , 1996 .

[152]  D James Surmeier,et al.  Recurrent Collateral Connections of Striatal Medium Spiny Neurons Are Disrupted in Models of Parkinson's Disease , 2008, The Journal of Neuroscience.

[153]  Yuchun Zhang,et al.  Involvement of Ih in Dopamine Modulation of Tonic Firing in Striatal Cholinergic Interneurons , 2007, The Journal of Neuroscience.

[154]  J. Tepper,et al.  Differential Dopaminergic Modulation of Neostriatal Synaptic Connections of Striatopallidal Axon Collaterals , 2009, The Journal of Neuroscience.

[155]  B. Bloch,et al.  Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[157]  O. Sporns,et al.  Motifs in Brain Networks , 2004, PLoS biology.

[158]  Daniel Lehmann,et al.  Modeling Compositionality by Dynamic Binding of Synfire Chains , 2004, Journal of Computational Neuroscience.

[159]  Joshua L. Plotkin,et al.  Synaptically driven state transitions in distal dendrites of striatal spiny neurons , 2011, Nature Neuroscience.

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

[161]  M. Pangalos,et al.  Loss of Retrograde Endocannabinoid Signaling and Reduced Adult Neurogenesis in Diacylglycerol Lipase Knock-out Mice , 2010, The Journal of Neuroscience.

[162]  G. Buzsáki,et al.  Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies , 2006, Neuron.

[163]  Rui M. Costa,et al.  Rapid Alterations in Corticostriatal Ensemble Coordination during Acute Dopamine-Dependent Motor Dysfunction , 2006, Neuron.

[164]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[165]  J. Seamans,et al.  Dopamine Receptor Signaling , 2004, Journal of receptor and signal transduction research.

[166]  P. Greengard,et al.  Regulation of phosphorylation of the GluR1 AMPA receptor by dopamine D2 receptors , 2006, Journal of neurochemistry.

[167]  Bert Sakmann,et al.  Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex , 2005, The Journal of Neuroscience.

[168]  Anatol C. Kreitzer,et al.  Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways , 2010, The Journal of Neuroscience.

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

[170]  Michael A. Arbib,et al.  The handbook of brain theory and neural networks , 1995, A Bradford book.

[171]  Sten Grillner,et al.  Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion , 2006, Neuron.

[172]  P. Greengard,et al.  Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons , 1995, Neuron.

[173]  J. Bargas,et al.  D2 Dopamine Receptors in Striatal Medium Spiny Neurons Reduce L-Type Ca2+ Currents and Excitability via a Novel PLCβ1–IP3–Calcineurin-Signaling Cascade , 2000, The Journal of Neuroscience.

[174]  Martin Parent,et al.  Single‐axon tracing study of corticostriatal projections arising from primary motor cortex in primates , 2006, The Journal of comparative neurology.

[175]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[176]  F. Gonon,et al.  D2 receptor stimulation, but not D1, restores striatal equilibrium in a rat model of Parkinsonism , 2009, Neurobiology of Disease.

[177]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[178]  D. Lovinger,et al.  Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill , 2009, Nature Neuroscience.

[179]  J. Girault,et al.  Modulation of the voltage‐gated sodium current in rat striatal neurons by DARPP‐32, an inhibitor of protein phosphatase , 1998, The European journal of neuroscience.

[180]  G. Bernardi,et al.  Impaired striatal D2 receptor function leads to enhanced GABA transmission in a mouse model of DYT1 dystonia , 2009, Neurobiology of Disease.

[181]  Y. Sakurai,et al.  Hippocampal and neocortical cell assemblies encode memory processes for different types of stimuli in the rat , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[182]  J. Sweatt,et al.  Mitogen-activated protein kinases in synaptic plasticity and memory , 2004, Current Opinion in Neurobiology.

[183]  D. James Surmeier,et al.  Corticostriatal and Thalamostriatal Synapses Have Distinctive Properties , 2008, The Journal of Neuroscience.

[184]  Masahiko Watanabe,et al.  The Endocannabinoid 2-Arachidonoylglycerol Produced by Diacylglycerol Lipase α Mediates Retrograde Suppression of Synaptic Transmission , 2010, Neuron.

[185]  Anatol C. Kreitzer,et al.  Striatal Plasticity and Basal Ganglia Circuit Function , 2008, Neuron.

[186]  Jeffery R Wickens,et al.  Inhibitory interactions between spiny projection neurons in the rat striatum. , 2002, Journal of neurophysiology.

[187]  Marc Flajolet,et al.  FGF acts as a co-transmitter through adenosine A2A receptor to regulate synaptic plasticity , 2008, Nature Neuroscience.

[188]  Nace L. Golding,et al.  Dendritic spikes as a mechanism for cooperative long-term potentiation , 2002, Nature.

[189]  Yu Tian Wang,et al.  Dual Regulation of NMDA Receptor Functions by Direct Protein-Protein Interactions with the Dopamine D1 Receptor , 2002, Cell.

[190]  J. Wickens.  Synaptic plasticity in the basal ganglia , 2009, Behavioural Brain Research.

[191]  Fiona E. N. LeBeau,et al.  Microcircuits in action – from CPGs to neocortex , 2005, Trends in Neurosciences.

[192]  Angus C Nairn,et al.  DARPP-32: an integrator of neurotransmission. , 2004, Annual review of pharmacology and toxicology.

[193]  J C Liu,et al.  Dopamine-modulated potassium channels on rat striatal neurons: specific activation and cellular expression , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[194]  R. P. Sullivan,et al.  Optogenetic control of striatal dopamine release in rats , 2010, Journal of neurochemistry.

[195]  J. Bargas,et al.  Cholinergic control of firing pattern and neurotransmission in rat neostriatal projection neurons: role of CaV2.1 and CaV2.2 Ca2+ channels. , 2005, Journal of neurophysiology.

[196]  R. Malenka,et al.  Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. , 1998, Journal of neurophysiology.

[197]  Talia N. Lerner,et al.  Endocannabinoid Signaling Mediates Psychomotor Activation by Adenosine A2A Antagonists , 2010, The Journal of Neuroscience.

[198]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[199]  A. Graybiel.  Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

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

[201]  Christian R. Huyck,et al.  Cell Assemblies as an Intermediate Level Model of Cognition , 2001, Emergent Neural Computational Architectures Based on Neuroscience.

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

[203]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[204]  P. Goldman-Rakic,et al.  Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[205]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[206]  E. Abercrombie,et al.  Spontaneous release of acetylcholine in striatum is preferentially regulated by inhibitory dopamine D2 receptors. , 1996, European journal of pharmacology.

[207]  J. Mink.  The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. , 2003, Archives of neurology.

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

[209]  E. Callaway,et al.  Excitatory cortical neurons form fine-scale functional networks , 2005, Nature.