Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action

Recent behavioral studies in both humans and rodents have found evidence that performance in decision-making tasks depends on two different learning processes; one encoding the relationship between actions and their consequences and a second involving the formation of stimulus–response associations. These learning processes are thought to govern goal-directed and habitual actions, respectively, and have been found to depend on homologous corticostriatal networks in these species. Thus, recent research using comparable behavioral tasks in both humans and rats has implicated homologous regions of cortex (medial prefrontal cortex/medial orbital cortex in humans and prelimbic cortex in rats) and of dorsal striatum (anterior caudate in humans and dorsomedial striatum in rats) in goal-directed action and in the control of habitual actions (posterior lateral putamen in humans and dorsolateral striatum in rats). These learning processes have been argued to be antagonistic or competing because their control over performance appears to be all or none. Nevertheless, evidence has started to accumulate suggesting that they may at times compete and at others cooperate in the selection and subsequent evaluation of actions necessary for normal choice performance. It appears likely that cooperation or competition between these sources of action control depends not only on local interactions in dorsal striatum but also on the cortico-basal ganglia network within which the striatum is embedded and that mediates the integration of learning with basic motivational and emotional processes. The neural basis of the integration of learning and motivation in choice and decision-making is still controversial and we review some recent hypotheses relating to this issue.

[1]  B. Skinner,et al.  Principles of Behavior , 1944 .

[2]  C. L. Hull Principles of Behavior , 1945 .

[3]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[4]  J. Deese The psychology of learning , 1952 .

[5]  C. Burt THE PSYCHOLOGY OF LEARNING , 1958 .

[6]  G D ELLISON,et al.  Separation of the Salivary and Motor Responses in Instrumental Conditioning , 1964, Science.

[7]  R. Rescorla A theory of pavlovian conditioning: The effectiveness of reinforcement and non-reinforcement , 1972 .

[8]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[9]  G. P. Smith,et al.  Efferent connections and nigral afferents of the nucleus accumbens septi in the rat , 1978, Neuroscience.

[10]  R. Hendersen,et al.  Avoidance of heat by rats: Effects of thermal context on rapidity of extinction , 1979 .

[11]  L. J. Hammond The effect of contingency upon the appetitive conditioning of free-operant behavior. , 1980, Journal of the experimental analysis of behavior.

[12]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[13]  Christopher D. Adams,et al.  Instrumental Responding following Reinforcer Devaluation , 1981 .

[14]  Christopher D. Adams Variations in the Sensitivity of Instrumental Responding to Reinforcer Devaluation , 1982 .

[15]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.

[16]  Edward A. Wasserman,et al.  Perception of causal relations in humans: Factors affecting judgments of response-outcome contingencies under free-operant procedures☆ , 1983 .

[17]  R. Rescorla,et al.  Postconditioning devaluation of a reinforcer affects instrumental responding. , 1985 .

[18]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[19]  R. Rescorla,et al.  Associative Structures In Instrumental Learning , 1986 .

[20]  B. Everitt,et al.  Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): II. Effects of preoptic area lesions, castration, and testosterone. , 1987, Journal of comparative psychology.

[21]  R. Oades,et al.  Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity , 1987, Brain Research Reviews.

[22]  Leonard S. Zegans,et al.  Neurology and psychiatry : a meeting of minds , 1989 .

[23]  A. Dickinson,et al.  Reinforcer specificity of the suppression of instrumental performance on a non-contingent schedule , 1989, Behavioural Processes.

[24]  B. Williams The effects of response contingency and reinforcement identity on response suppression by alternative reinforcement , 1989 .

[25]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[26]  B. Balleine,et al.  Incentive learning and the motivational control of instrumental performance by thirst , 1989 .

[27]  Cathleen Conzales,et al.  Amygdalonigral pathway: An anterograde study in the rat with Phaseolus vulgaris leucoagglutinin (PHA‐L) , 1990, The Journal of comparative neurology.

[28]  Robert A. Rescorla,et al.  Effect of reinforcer devaluation on discriminative control of instrumental behavior. , 1990, Journal of experimental psychology. Animal behavior processes.

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

[30]  H. Groenewegen,et al.  The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. , 1990, Progress in brain research.

[31]  A. Dickinson,et al.  Instrumental judgment and performance under variations in action-outcome contingency and contiguity , 1991, Memory & cognition.

[32]  B. Balleine,et al.  Instrumental Performance following Reinforcer Devaluation Depends upon Incentive Learning , 1991 .

[33]  P. Goldman-Rakic,et al.  Distribution of dopaminergic receptors in the primate cerebral cortex: Quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390 , 1991, Neuroscience.

[34]  G. Percheron,et al.  Parallel processing in the basal ganglia: up to a point , 1991, Trends in Neurosciences.

[35]  B. Balleine Instrumental performance following a shift in primary motivation depends on incentive learning. , 1992, Journal of experimental psychology. Animal behavior processes.

[36]  J. Kaas,et al.  Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys , 1992, The Journal of comparative neurology.

[37]  Donald A. Sofge,et al.  Handbook of Intelligent Control: Neural, Fuzzy, and Adaptive Approaches , 1992 .

[38]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[39]  W. Nauta Reciprocal Links of the Corpus striatum with the Cerebral Cortex and Limbic System: A Common Substrate for Movement and Thought? , 1993 .

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

[41]  S. Haber,et al.  Primate striatonigral projections: A comparison of the sensorimotor‐related striatum and the ventral striatum , 1994, The Journal of comparative neurology.

[42]  B. Balleine,et al.  Effects of ibotenic acid lesions of the Nucleus Accumbens on instrumental action , 1994, Behavioural Brain Research.

[43]  B. Balleine,et al.  Role of cholecystokinin in the motivational control of instrumental action in rats. , 1994, Behavioral neuroscience.

[44]  W. Schultz,et al.  Importance of unpredictability for reward responses in primate dopamine neurons. , 1994, Journal of neurophysiology.

[45]  R. Rescorla Transfer of instrumental control mediated by a devalued outcome , 1994 .

[46]  B. Balleine,et al.  Benzodiazepine-induced outcome revaluation and the motivational control of instrumental action in rats. , 1994, Behavioral neuroscience.

[47]  J. Saint-Cyr,et al.  Behavior and the basal ganglia. , 1995, Advances in neurology.

[48]  B. Balleine,et al.  Cholecystokinin attenuates incentive learning in rats. , 1995, Behavioral neuroscience.

[49]  T. Preuss Do Rats Have Prefrontal Cortex? The Rose-Woolsey-Akert Program Reconsidered , 1995, Journal of Cognitive Neuroscience.

[50]  R. Boakes,et al.  Motivational control after extended instrumental training , 1995 .

[51]  A. Barto,et al.  Adaptive Critics and the Basal Ganglia , 1994 .

[52]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[53]  E. Audinat,et al.  Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents , 1995, The Journal of comparative neurology.

[54]  P. Dayan,et al.  A framework for mesencephalic dopamine systems based on predictive Hebbian learning , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  S. Woods,et al.  Behavioral, endocrine, and hypothalamic responses to involuntary overfeeding. , 1996, The American journal of physiology.

[56]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[57]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

[58]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

[59]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[60]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. II. Subcortical structures and learning by trial and error. , 1997, Journal of neurophysiology.

[61]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

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

[63]  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.

[64]  A. Dickinson,et al.  Omission Learning after Instrumental Pretraining , 1998 .

[65]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[66]  J. Hollerman,et al.  Dopamine neurons report an error in the temporal prediction of reward during learning , 1998, Nature Neuroscience.

[67]  B. Balleine,et al.  The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety , 1998 .

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

[69]  B. Levin Arcuate NPY neurons and energy homeostasis in diet-induced obese and resistant rats. , 1999, The American journal of physiology.

[70]  T. Robbins,et al.  Dissociation in Effects of Lesions of the Nucleus Accumbens Core and Shell on Appetitive Pavlovian Approach Behavior and the Potentiation of Conditioned Reinforcement and Locomotor Activity byd-Amphetamine , 1999, The Journal of Neuroscience.

[71]  H. Groenewegen,et al.  Integration and segregation of limbic cortico-striatal loops at the thalamic level: an experimental tracing study in rats , 1999, Journal of Chemical Neuroanatomy.

[72]  W. Schultz,et al.  Relative reward preference in primate orbitofrontal cortex , 1999, Nature.

[73]  E T Rolls,et al.  Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. , 2000, Neuroreport.

[74]  J. Mirenowicz,et al.  Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. , 2000, Behavioral neuroscience.

[75]  S. Klein,et al.  Handbook of contemporary learning theories , 2000 .

[76]  S. Woods,et al.  Food intake and the regulation of body weight. , 2000, Annual review of psychology.

[77]  E T Rolls,et al.  Sensory‐specific satiety‐related olfactory activation of the human orbitofrontal cortex , 2000, Neuroreport.

[78]  B. Everitt,et al.  Limbic cortical-ventral striatal systems underlying appetitive conditioning. , 2000, Progress in brain research.

[79]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[80]  J. Mitrofanis,et al.  Organisation of the amygdalo-thalamic pathways in rats , 2000, Anatomy and Embryology.

[81]  B. Balleine,et al.  The Effect of Lesions of the Insular Cortex on Instrumental Conditioning: Evidence for a Role in Incentive Memory , 2000, The Journal of Neuroscience.

[82]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[83]  K. Berridge,et al.  Intra-Accumbens Amphetamine Increases the Conditioned Incentive Salience of Sucrose Reward: Enhancement of Reward “Wanting” without Enhanced “Liking” or Response Reinforcement , 2000, The Journal of Neuroscience.

[84]  D. S. Zahm,et al.  An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens , 2000, Neuroscience & Biobehavioral Reviews.

[85]  D. Joel,et al.  The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum , 2000, Neuroscience.

[86]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[87]  A. Dickinson,et al.  Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour , 2001, The European journal of neuroscience.

[88]  Nikolaus R. McFarland,et al.  The Place of the Thalamus in Frontal Cortical-Basal Ganglia Circuits , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[90]  K. Doya,et al.  Parallel Cortico-Basal Ganglia Mechanisms for Acquisition and Execution of Visuomotor SequencesA Computational Approach , 2001, Journal of Cognitive Neuroscience.

[91]  A. Dickinson,et al.  The role of withdrawal in heroin addiction: enhances reward or promotes avoidance? , 2001, Nature Neuroscience.

[92]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[93]  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.

[94]  D. Joel,et al.  Open interconnected model of basal ganglia‐thalamocortical circuitry and its relevance to the clinical syndrome of Huntington's disease , 2001, Movement disorders : official journal of the Movement Disorder Society.

[95]  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.

[96]  E. Rolls,et al.  Representation of pleasant and aversive taste in the human brain. , 2001, Journal of neurophysiology.

[97]  B. Balleine,et al.  An Assessment of Factors Contributing to Instrumental Performance for Sexual Reward in the Rat , 2002, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[98]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[99]  P. Holland,et al.  Amygdalo-Hypothalamic Circuit Allows Learned Cues to Override Satiety and Promote Eating , 2002, The Journal of Neuroscience.

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

[101]  J. O'Doherty,et al.  Appetitive and Aversive Olfactory Learning in Humans Studied Using Event-Related Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[102]  P. Holland,et al.  The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats , 2002, Physiology & Behavior.

[103]  Eytan Ruppin,et al.  Actor-critic models of the basal ganglia: new anatomical and computational perspectives , 2002, Neural Networks.

[104]  T. Robbins,et al.  Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function , 2002, Behavioural Brain Research.

[105]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[106]  V. Brown,et al.  Rodent models of prefrontal cortical function , 2002, Trends in Neurosciences.

[107]  J. N. P. Rawlins,et al.  Effects of cytotoxic nucleus accumbens lesions on instrumental conditioning in rats , 2002, Experimental Brain Research.

[108]  B. Balleine,et al.  The Role of Learning in the Operation of Motivational Systems , 2002 .

[109]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[110]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

[111]  E. Rolls,et al.  Different representations of pleasant and unpleasant odours in the human brain , 2003, The European journal of neuroscience.

[112]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[113]  E. Rolls,et al.  Human cortical responses to water in the mouth, and the effects of thirst. , 2003, Journal of neurophysiology.

[114]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[115]  G. Alheid Extended Amygdala and Basal Forebrain , 2003, Annals of the New York Academy of Sciences.

[116]  Samuel M. McClure,et al.  Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum , 2003, Neuron.

[117]  P. Holland,et al.  Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus‐potentiated feeding and Pavlovian‐instrumental transfer , 2003, The European journal of neuroscience.

[118]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

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

[120]  Karl J. Friston,et al.  Temporal Difference Models and Reward-Related Learning in the Human Brain , 2003, Neuron.

[121]  B. Kolb,et al.  Do rats have a prefrontal cortex? , 2003, Behavioural Brain Research.

[122]  B. Balleine,et al.  The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning , 2003, The Journal of Neuroscience.

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

[124]  J. Fudge,et al.  The extended amygdala and the dopamine system: another piece of the dopamine puzzle. , 2003, The Journal of neuropsychiatry and clinical neurosciences.

[125]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[126]  B. Balleine,et al.  Instrumental and Pavlovian incentive processes have dissociable effects on components of a heterogeneous instrumental chain. , 2003, Journal of experimental psychology. Animal behavior processes.

[127]  H. Bergman,et al.  Information processing, dimensionality reduction and reinforcement learning in the basal ganglia , 2003, Progress in Neurobiology.

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

[129]  A. Dickinson,et al.  The Interaction between Discriminative Stimuli and Outcomes during Instrumental Learning , 2003, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[130]  Geoffrey Schoenbaum,et al.  Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task , 2003, The Journal of Neuroscience.

[131]  P. Holland Relations between Pavlovian-instrumental transfer and reinforcer devaluation. , 2004, Journal of experimental psychology. Animal behavior processes.

[132]  Saori C. Tanaka,et al.  Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops , 2004, Nature Neuroscience.

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

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

[135]  A. Kelley Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning , 2004, Neuroscience & Biobehavioral Reviews.

[136]  V. Routh,et al.  The regulation of glucose-excited neurons in the hypothalamic arcuate nucleus by glucose and feeding-relevant peptides. , 2004, Diabetes.

[137]  I. Q. Wishaw,et al.  THE BEHAVIOR OF THE LABORATORY RAT A Handbook with Tests , 2004 .

[138]  M. Packard,et al.  Habit learning in Tourette syndrome: a translational neuroscience approach to a developmental psychopathology. , 2004, Archives of general psychiatry.

[139]  James M Kilner,et al.  Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala , 2005, The Journal of Neuroscience.

[140]  T. Stanford,et al.  Subcortical loops through the basal ganglia , 2005, Trends in Neurosciences.

[141]  A. Faure,et al.  Lesion to the Nigrostriatal Dopamine System Disrupts Stimulus-Response Habit Formation , 2005, The Journal of Neuroscience.

[142]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[143]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[145]  B. Balleine,et al.  Double Dissociation of Basolateral and Central Amygdala Lesions on the General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer , 2005, The Journal of Neuroscience.

[146]  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.

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

[148]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[149]  B. Everitt,et al.  Acquisition of Instrumental Conditioned Reinforcement is Resistant to the Devaluation of the Unconditioned Stimulus , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

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

[151]  B. Balleine,et al.  Consolidation and Reconsolidation of Incentive Learning in the Amygdala , 2005, The Journal of Neuroscience.

[152]  E. Abercrombie,et al.  Thalamic regulation of striatal acetylcholine efflux is both direct and indirect and qualitatively altered in the dopamine-depleted striatum , 2005, Neuroscience.

[153]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[154]  B. Balleine,et al.  Dorsomedial Prefrontal Cortex Resolves Response Conflict in Rats , 2006, The Journal of Neuroscience.

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

[156]  M. Roitman,et al.  Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm , 2006, The European journal of neuroscience.

[157]  Erwan Bezard,et al.  Phenotype of Striatofugal Medium Spiny Neurons in Parkinsonian and Dyskinetic Nonhuman Primates: A Call for a Reappraisal of the Functional Organization of the Basal Ganglia , 2006, The Journal of Neuroscience.

[158]  J. O'Doherty,et al.  Is Avoiding an Aversive Outcome Rewarding? Neural Substrates of Avoidance Learning in the Human Brain , 2006, PLoS biology.

[159]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[160]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[161]  R. Dolan,et al.  Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans , 2006, Nature.

[162]  Mitsuo Kawato,et al.  Heterarchical reinforcement-learning model for integration of multiple cortico-striatal loops: fMRI examination in stimulus-action-reward association learning , 2006, Neural Networks.

[163]  W. Hauber,et al.  Inactivation of the ventral tegmental area abolished the general excitatory influence of Pavlovian cues on instrumental performance. , 2006, Learning & memory.

[164]  J. O'Doherty,et al.  The Role of the Ventromedial Prefrontal Cortex in Abstract State-Based Inference during Decision Making in Humans , 2006, The Journal of Neuroscience.

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

[166]  M. Frank,et al.  Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. , 2006, Psychological review.

[167]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

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

[169]  A. Dickinson,et al.  Motivational control of heroin seeking by conditioned stimuli associated with withdrawal and heroin taking by rats. , 2006, Behavioral neuroscience.

[170]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[171]  N. Daw,et al.  Reinforcement Learning Signals in the Human Striatum Distinguish Learners from Nonlearners during Reward-Based Decision Making , 2007, The Journal of Neuroscience.

[172]  P. Janak,et al.  Inactivation of the Lateral But Not Medial Dorsal Striatum Eliminates the Excitatory Impact of Pavlovian Stimuli on Instrumental Responding , 2007, The Journal of Neuroscience.

[173]  J. O'Doherty,et al.  Orbitofrontal Cortex Encodes Willingness to Pay in Everyday Economic Transactions , 2007, The Journal of Neuroscience.

[174]  B. Balleine,et al.  Orbitofrontal Cortex Mediates Outcome Encoding in Pavlovian But Not Instrumental Conditioning , 2007, The Journal of Neuroscience.

[175]  Vivian V. Valentin,et al.  Determining the Neural Substrates of Goal-Directed Learning in the Human Brain , 2007, The Journal of Neuroscience.

[176]  P. Holland,et al.  Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation , 2007, The European journal of neuroscience.

[177]  B. Balleine,et al.  Still at the Choice‐Point , 2007, Annals of the New York Academy of Sciences.

[178]  R. Carelli,et al.  The Nucleus Accumbens and Pavlovian Reward Learning , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[179]  Thomas E. Hazy,et al.  Towards an executive without a homunculus: computational models of the prefrontal cortex/basal ganglia system , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[180]  J. Bolam,et al.  A Single-Cell Analysis of Intrinsic Connectivity in the Rat Globus Pallidus , 2007, The Journal of Neuroscience.

[181]  B. Balleine Reward and decision making in corticobasal ganglia networks , 2007 .

[182]  Bernard W Balleine,et al.  General and outcome‐specific forms of Pavlovian‐instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area , 2007, The European journal of neuroscience.

[183]  B. Balleine,et al.  Selective reinstatement of instrumental performance depends on the discriminative stimulus properties of the mediating outcome , 2007, Learning & behavior.

[184]  Alexander M. Benison,et al.  Auditory, somatosensory, and multisensory insular cortex in the rat. , 2008, Cerebral cortex.

[185]  B. Balleine,et al.  Differential Involvement of the Basolateral Amygdala and Mediodorsal Thalamus in Instrumental Action Selection , 2008, The Journal of Neuroscience.

[186]  B. Balleine,et al.  The Neural Mechanisms Underlying the Influence of Pavlovian Cues on Human Decision Making , 2008, The Journal of Neuroscience.

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

[188]  Colin Camerer,et al.  Dissociating the Role of the Orbitofrontal Cortex and the Striatum in the Computation of Goal Values and Prediction Errors , 2008, The Journal of Neuroscience.

[189]  Steven P. Wise,et al.  Forward frontal fields: phylogeny and fundamental function , 2008, Trends in Neurosciences.

[190]  B. Everitt,et al.  Cocaine Seeking Habits Depend upon Dopamine-Dependent Serial Connectivity Linking the Ventral with the Dorsal Striatum , 2008, Neuron.

[191]  A. Nambu Seven problems on the basal ganglia , 2008, Current Opinion in Neurobiology.

[192]  P. Dayan,et al.  Human Pavlovian–Instrumental Transfer , 2008, The Journal of Neuroscience.

[193]  Colin Camerer,et al.  Neuroeconomics: decision making and the brain , 2008 .

[194]  B. Balleine,et al.  Calculating Consequences: Brain Systems That Encode the Causal Effects of Actions , 2008, The Journal of Neuroscience.

[195]  B. Balleine,et al.  Reward‐guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico‐basal ganglia networks , 2008, The European journal of neuroscience.

[196]  B. Balleine,et al.  A specific role for posterior dorsolateral striatum in human habit learning , 2009, The European journal of neuroscience.

[197]  J. Gläscher,et al.  Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. , 2009, Cerebral cortex.

[198]  B. Balleine,et al.  Multiple Forms of Value Learning and the Function of Dopamine , 2009 .

[199]  B. Balleine,et al.  The integrative function of the basal ganglia in instrumental conditioning , 2009, Behavioural Brain Research.

[200]  Steve Reilly,et al.  Conditioned taste aversion : behavioral and neural processes , 2009 .

[201]  B. Balleine,et al.  Distinct opioid circuits determine the palatability and the desirability of rewarding events , 2009, Proceedings of the National Academy of Sciences.

[202]  A Theory of the Basal Ganglia and Their Disorders, R. Miller, Publishers CRC Press, Taylor & Francis Group (2008), Price: $164.95, ISBN: 1-4200-5897-5 , 2010 .

[203]  A. Dickinson Instrumental Conditioning , 2020, Encyclopedia of Evolutionary Psychological Science.

[204]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[205]  K. Campbell,et al.  A neural correlate of response bias in monkey caudate nucleus , 2022 .