A specific role for posterior dorsolateral striatum in human habit learning

Habits are characterized by an insensitivity to their consequences and, as such, can be distinguished from goal‐directed actions. The neural basis of the development of demonstrably outcome‐insensitive habitual actions in humans has not been previously characterized. In this experiment, we show that extensive training on a free‐operant task reduces the sensitivity of participants’ behavior to a reduction in outcome value. Analysis of functional magnetic resonance imaging data acquired during training revealed a significant increase in task‐related cue sensitivity in a right posterior putamen–globus pallidus region as training progressed. These results provide evidence for a shift from goal‐directed to habit‐based control of instrumental actions in humans, and suggest that cue‐driven activation in a specific region of dorsolateral posterior putamen may contribute to the habitual control of behavior in humans.

[1]  Rheumatic Heart Disease in Dewsbury , 1937, British medical journal.

[2]  B. Gandevia,et al.  DECLARATION OF HELSINKI. , 1964, The Medical journal of Australia.

[3]  Rickham Pp.  Human Experimentation: Code of Ethics of the World Medical Association (Declaration of Helsinki). , 1964, Canadian Medical Association journal.

[4]  P. P. Rickham.  HUMAN EXPERIMENTATION. CODE OF ETHICS OF THE WORLD MEDICAL ASSOCIATION. DECLARATION OF HELSINKI. , 1964, British medical journal.

[5]  D. Garner,et al.  The Eating Attitudes Test: psychometric features and clinical correlates , 1982, Psychological Medicine.

[6]  Christopher D. Adams,et al.  The Effect of the Instrumental Training Contingency on Susceptibility to Reinforcer Devaluation , 1983 .

[7]  E. Rolls,et al.  Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man , 1983, Physiology & Behavior.

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

[9]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

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

[11]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[12]  S. Haber,et al.  Ventral pallidostriatal pathway in the monkey: evidence for modulation of basal ganglia circuits. , 1996, The Journal of comparative neurology.

[13]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[14]  P. Strick,et al.  The temporal lobe is a target of output from the basal ganglia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

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

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

[20]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[21]  Ann M Graybiel,et al.  Toward a Neurobiology of Obsessive-Compulsive Disorder , 2000, Neuron.

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

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

[24]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

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

[26]  S. Killcross,et al.  Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats , 2003, Behavioural Brain Research.

[27]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

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

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

[31]  Jaap Oosterlaan,et al.  Pathological gambling: a comprehensive review of biobehavioral findings , 2004, Neuroscience & Biobehavioral Reviews.

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

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

[34]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[35]  L. Squire,et al.  Robust habit learning in the absence of awareness and independent of the medial temporal lobe , 2005, Nature.

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

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

[38]  R. Deichmann,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex: compensation of susceptibility-induced gradients in the readout direction , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[39]  M. Balestrieri,et al.  The EAT-26 as screening instrument for clinical nutrition unit attenders , 2006, International Journal of Obesity.

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

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

[42]  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.

[43]  Russell A Poldrack,et al.  Modulation of competing memory systems by distraction. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[46]  B. Balleine,et al.  Action Selection and Initiation in Instrumental Conditioning , 2007 .

[47]  M. Roesch,et al.  Neuronal Activity Related to Anticipated Reward in Frontal Cortex , 2007, Annals of the New York Academy of Sciences.

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

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