The Role of the Dorsal Striatum in Reward and Decision-Making

Although the involvement in the striatum in the refinement and control of motor movement has long been recognized, recent description of discrete frontal corticobasal ganglia networks in a range of species has focused attention on the role particularly of the dorsal striatum in executive functions. Current evidence suggests that the dorsal striatum contributes directly to decision-making, especially to action selection and initiation, through the integration of sensorimotor, cognitive, and motivational/emotional information within specific corticostriatal circuits involving discrete regions of striatum. We review key evidence from recent studies in rodent, nonhuman primate, and human subjects.

[1]  H. Künzle Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[2]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[3]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[4]  B. Balleine,et al.  Motivational control of goal-directed action , 1994 .

[5]  Joel L. Davis,et al.  A Model of How the Basal Ganglia Generate and Use Neural Signals That Predict Reinforcement , 1994 .

[6]  A. Graybiel,et al.  Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M Ashtari,et al.  Reduced caudate nucleus volume in obsessive-compulsive disorder. , 1995, Archives of general psychiatry.

[8]  P. Goldman-Rakic Architecture of the Prefrontal Cortex and the Central Executive , 1995, Annals of the New York Academy of Sciences.

[9]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[10]  B. Richmond,et al.  Neuronal Signals in the Monkey Ventral Striatum Related to Progress through a Predictable Series of Trials , 1998, The Journal of Neuroscience.

[11]  J. Hollerman,et al.  Influence of reward expectation on behavior-related neuronal activity in primate striatum. , 1998, Journal of neurophysiology.

[12]  B. Balleine,et al.  Goal-directed instrumental action: contingency and incentive learning and their cortical substrates , 1998, Neuropharmacology.

[13]  D. Brooks,et al.  Evidence for striatal dopamine release during a video game , 1998, Nature.

[14]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[15]  J. Hollerman,et al.  Modifications of reward expectation-related neuronal activity during learning in primate striatum. , 1998, Journal of neurophysiology.

[16]  C. I. Connolly,et al.  Building neural representations of habits. , 1999, Science.

[17]  J. Partridge,et al.  Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. , 2000, Journal of neurophysiology.

[18]  L. Nystrom,et al.  Tracking the hemodynamic responses to reward and punishment in the striatum. , 2000, Journal of neurophysiology.

[19]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[20]  S. Mcconnell,et al.  NudC Associates with Lis1 and the Dynein Motor at the Leading Pole of Neurons , 2001, The Journal of Neuroscience.

[21]  J. Galen Buckwalter,et al.  Regional differences in the expression of corticostriatal synaptic plasticity , 2001, Neuroscience.

[22]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[23]  B. Balleine,et al.  The Role of the Nucleus Accumbens in Instrumental Conditioning: Evidence of a Functional Dissociation between Accumbens Core and Shell , 2001, The Journal of Neuroscience.

[24]  A. Smit,et al.  Synapse Formation between Central Neurons Requires Postsynaptic Expression of the MEN1 Tumor Suppressor Gene , 2001, The Journal of Neuroscience.

[25]  L. Chen,et al.  Neuronal responses in the frontal cortico-basal ganglia system during delayed matching-to-sample task: ensemble recording in freely moving rats , 2001, Experimental Brain Research.

[26]  F. Fazio,et al.  The status of dopamine nerve terminals in Parkinson's disease and essential tremor: a PET study with the tracer [11-C]FE-CIT , 2001, Neurological Sciences.

[27]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[28]  O. Hikosaka,et al.  A neural correlate of response bias in monkey caudate nucleus , 2002, Nature.

[29]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[30]  O. Hikosaka,et al.  Differential activation of monkey striatal neurons in the early and late stages of procedural learning , 2002, Experimental Brain Research.

[31]  P. Dayan,et al.  Reward, Motivation, and Reinforcement Learning , 2002, Neuron.

[32]  N. Volkow,et al.  “Nonhedonic” food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect , 2002, Synapse.

[33]  A. Graybiel,et al.  A Network Representation of Response Probability in the Striatum , 2002, Neuron.

[34]  John N. J. Reynolds,et al.  Dopamine-dependent plasticity of corticostriatal synapses , 2002, Neural Networks.

[35]  T. Robbins,et al.  Dopamine Release in the Dorsal Striatum during Cocaine-Seeking Behavior under the Control of a Drug-Associated Cue , 2002, The Journal of Neuroscience.

[36]  G. Pagnoni,et al.  A Neural Basis for Social Cooperation , 2002, Neuron.

[37]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[38]  B. Balleine,et al.  The role of prelimbic cortex in instrumental conditioning , 2003, Behavioural Brain Research.

[39]  D. Boussaoud,et al.  Neuronal activity in the monkey striatum during conditional visuomotor learning , 2003, Experimental Brain Research.

[40]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[41]  S. Wise,et al.  Comparison of learning‐related neuronal activity in the dorsal premotor cortex and striatum , 2004, The European journal of neuroscience.

[42]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[43]  D. D. de Quervain,et al.  The Neural Basis of Altruistic Punishment , 2004, Science.

[44]  M. Gluck,et al.  Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. , 2004, Brain : a journal of neurology.

[45]  M. Nicolelis,et al.  Differential Corticostriatal Plasticity during Fast and Slow Motor Skill Learning in Mice , 2004, Current Biology.

[46]  F. McGlone,et al.  Dopamine Transmission in the Human Striatum during Monetary Reward Tasks , 2004, The Journal of Neuroscience.

[47]  B. Balleine,et al.  Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning , 2004, The European journal of neuroscience.

[48]  K. Doya,et al.  A Neural Correlate of Reward-Based Behavioral Learning in Caudate Nucleus: A Functional Magnetic Resonance Imaging Study of a Stochastic Decision Task , 2004, The Journal of Neuroscience.

[49]  M. Delgado,et al.  Modulation of Caudate Activity by Action Contingency , 2004, Neuron.

[50]  Aziz M. Ulug,et al.  Differential cingulate and caudate activation following unexpected nonrewarding stimuli , 2004, NeuroImage.

[51]  J. O'Doherty,et al.  Reward representations and reward-related learning in the human brain: insights from neuroimaging , 2004, Current Opinion in Neurobiology.

[52]  A. Graybiel,et al.  Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories , 2005, Nature.

[53]  S. Quartz,et al.  Getting to Know You: Reputation and Trust in a Two-Person Economic Exchange , 2005, Science.

[54]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[55]  M. Delgado,et al.  Perceptions of moral character modulate the neural systems of reward during the trust game , 2005, Nature Neuroscience.

[56]  Karl J. Friston,et al.  Opponent appetitive-aversive neural processes underlie predictive learning of pain relief , 2005, Nature Neuroscience.

[57]  Paul Leonard Gabbott,et al.  Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers , 2005, The Journal of comparative neurology.

[58]  P. Dayan,et al.  Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control , 2005, Nature Neuroscience.

[59]  B. Balleine,et al.  Lesions of Medial Prefrontal Cortex Disrupt the Acquisition But Not the Expression of Goal-Directed Learning , 2005, The Journal of Neuroscience.

[60]  B. Balleine Neural bases of food-seeking: Affect, arousal and reward in corticostriatolimbic circuits , 2005, Physiology & Behavior.

[61]  B. Balleine,et al.  The role of the dorsomedial striatum in instrumental conditioning , 2005, The European journal of neuroscience.

[62]  Hongtu Zhu,et al.  Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome , 2005, Neurology.

[63]  S. Inati,et al.  An fMRI study of reward-related probability learning , 2005, NeuroImage.

[64]  B. Balleine,et al.  Blockade of NMDA receptors in the dorsomedial striatum prevents action–outcome learning in instrumental conditioning , 2005, The European journal of neuroscience.

[65]  M. Kawato,et al.  Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. , 2006, Journal of neurophysiology.

[66]  A. Kelley,et al.  Dynamic shifts in corticostriatal expression patterns of the immediate early genes Homer 1a and Zif268 during early and late phases of instrumental training. , 2006, Learning & memory.

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

[68]  J. Olson,et al.  Regional and cellular gene expression changes in human Huntington's disease brain. , 2006, Human molecular genetics.

[69]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[70]  Ziv M. Williams,et al.  Selective enhancement of associative learning by microstimulation of the anterior caudate , 2006, Nature Neuroscience.

[71]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

[72]  W. Poewe,et al.  Topography of putaminal degeneration in multiple system atrophy: A diffusion magnetic resonance study , 2006, Movement disorders : official journal of the Movement Disorder Society.

[73]  Kae Nakamura,et al.  Facilitation of Saccadic Eye Movements by Postsaccadic Electrical Stimulation in the Primate Caudate , 2006, The Journal of Neuroscience.

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

[75]  Kenji Doya,et al.  Brain mechanism of reward prediction under predictable and unpredictable environmental dynamics , 2006, Neural Networks.

[76]  B. Balleine,et al.  Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning , 2006, Behavioural Brain Research.

[77]  B. Dubois,et al.  Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. , 2006, Cerebral cortex.

[78]  M. West,et al.  Changes in activity of the striatum during formation of a motor habit , 2007, The European journal of neuroscience.