Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease

Progressive loss of the ascending dopaminergic projection in the basal ganglia is a fundamental pathological feature of Parkinson's disease. Studies in animals and humans have identified spatially segregated functional territories in the basal ganglia for the control of goal-directed and habitual actions. In patients with Parkinson's disease the loss of dopamine is predominantly in the posterior putamen, a region of the basal ganglia associated with the control of habitual behaviour. These patients may therefore be forced into a progressive reliance on the goal-directed mode of action control that is mediated by comparatively preserved processing in the rostromedial striatum. Thus, many of their behavioural difficulties may reflect a loss of normal automatic control owing to distorting output signals from habitual control circuits, which impede the expression of goal-directed action.

[1]  D. Ferrier The Functions of the Brain , 1887, Edinburgh Medical Journal.

[2]  S. A. Wilson PROGRESSIVE LENTICULAR DEGENERATION , 1912 .

[3]  S. A. Wilson,et al.  Disorders of motility and muscle tone with special reference to the corpus striatum , 1925 .

[4]  J. P. Martin HEMICHOREA RESULTING FROM A LOCAL LESION OF THE BRAIN. (THE SYNDROME OF THE BODY OF LUYS , 1927 .

[5]  J. P. Martin,et al.  HEMICHOREA ASSOCIATED WITH A LESION OF THE CORPUS LUYSII , 1934 .

[6]  J R WHITTIER,et al.  Analysis of choreoid hyperkinesia in the rhesus monkey. Surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus ol luys , 1950, The Journal of comparative neurology.

[7]  R S SCHWAB,et al.  Control of two simultaneous voluntary motor acts in normals and in parkinsonism. , 1954, A.M.A. archives of neurology and psychiatry.

[8]  I. McCaul,et al.  Acute hemiballismus treated by ventrolateral thalamolysis. , 1959, Brain : a journal of neurology.

[9]  O. Hornykiewicz,et al.  [Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system]. , 1998, Klinische Wochenschrift.

[10]  O. Hornykiewicz,et al.  [The L-3,4-dioxyphenylalanine (DOPA)-effect in Parkinson-akinesia]. , 1961, Wiener klinische Wochenschrift.

[11]  [L-dopa in Parkinson's syndrome]. , 1971 .

[12]  K. Spence Behavior Theory and Conditioning , 1978 .

[13]  R. Hassler Striatal control of locomotion, intentional actions and of integrating and perceptive activity , 1978, Journal of the Neurological Sciences.

[14]  M. Hallett,et al.  A physiological mechanism of bradykinesia. , 1980, Brain : a journal of neurology.

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

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

[17]  C. Marsden The mysterious motor function of the basal ganglia , 1982, Neurology.

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

[19]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. , 1985, Journal of neurophysiology.

[20]  G E Stelmach,et al.  Movement preparation in Parkinson's disease. The use of advance information. , 1986, Brain : a journal of neurology.

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

[22]  C. Marsden,et al.  Performance of simultaneous movements in patients with Parkinson's disease. , 1986, Brain : a journal of neurology.

[23]  J. Penney,et al.  Striatal inhomogeneities and basal ganglia function , 1986, Movement disorders : official journal of the Movement Disorder Society.

[24]  C. D. Stern,et al.  Handbook of Chemical Neuroanatomy Methods in Chemical Neuroanatomy. Edited by A. Bjorklund and T. Hokfelt. Elsevier, Amsterdam, 1983. Cloth bound, 548 pp. UK £140. (Volume 1 in the series). , 1986, Neurochemistry International.

[25]  C. Marsden,et al.  Disturbance of sequential movements in patients with Parkinson's disease. , 1987, Brain : a journal of neurology.

[26]  A. Crossman,et al.  Primate models of dyskinesia: The experimental approach to the study of basal ganglia-related involuntary movement disorders , 1987, Neuroscience.

[27]  S. Kish,et al.  Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. , 1988, The New England journal of medicine.

[28]  A. Parent,et al.  Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey , 1989, Brain Research.

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

[30]  O Hikosaka,et al.  Functional properties of monkey caudate neurons. II. Visual and auditory responses. , 1989, Journal of neurophysiology.

[31]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

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

[33]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[34]  M. Delong,et al.  Primate models of movement disorders of basal ganglia origin , 1990, Trends in Neurosciences.

[35]  Michael I. Jordan,et al.  Advances in Neural Information Processing Systems 30 , 1995 .

[36]  M. Kimura Behaviorally contingent property of movement-related activity of the primate putamen. , 1990, Journal of neurophysiology.

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

[38]  L. Tremblay,et al.  Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism , 1991, Brain Research.

[39]  A. Grace Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia , 1991, Neuroscience.

[40]  A. Lees,et al.  Ageing and Parkinson's disease: substantia nigra regional selectivity. , 1991, Brain : a journal of neurology.

[41]  C D Marsden,et al.  Simple and choice reaction time and the use of advance information for motor preparation in Parkinson's disease. , 1992, Brain : a journal of neurology.

[42]  A. Graybiel,et al.  Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[44]  J. Bolam,et al.  Convergent Synaptic Input From the Neostriatum and the Subthalamus Onto Identified Nigrothalamic Neurons in the Rat , 1994, The European journal of neuroscience.

[45]  M. Bevan,et al.  The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: A comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study , 1994, Neuroscience.

[46]  H. Bergman,et al.  Parkinsonian Tremor is Associated with Low Frequency Neuronal Oscillations in Selective Loops of the Basal Ganglia , 1994 .

[47]  C. Marsden,et al.  The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. , 1994, Brain : a journal of neurology.

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

[49]  D J Brooks,et al.  Clinical and [18F] dopa PET findings in early Parkinson's disease. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[50]  Y. Smith,et al.  The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey , 1996, Neuroscience.

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

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

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

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

[55]  R A Bakay,et al.  Microelectrode-guided pallidotomy: technical approach and its application in medically intractable Parkinson's disease. , 1998, Journal of neurosurgery.

[56]  W Spijkers,et al.  Effects of sleep loss, time of day, and extended mental work on implicit and explicit learning of sequences. , 1998, Journal of experimental psychology. Applied.

[57]  D. R. Smith,et al.  Behavioural assessment of mice lacking D1A dopamine receptors , 1998, Neuroscience.

[58]  O. Hornykiewicz,et al.  Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system. , 1960, Parkinsonism & related disorders.

[59]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

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

[61]  C. Marsden,et al.  What do the basal ganglia do? , 1998, The Lancet.

[62]  R Iansek,et al.  Provision of external cues and movement sequencing in Parkinson's disease. , 1998, Motor control.

[63]  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.

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

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

[66]  Y. Smith,et al.  Microcircuitry of the direct and indirect pathways of the basal ganglia. , 1998, Neuroscience.

[67]  H. Kita,et al.  Monkey globus pallidus external segment neurons projecting to the neostriatum. , 1999, Neuroreport.

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

[69]  J. Lanciego,et al.  Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: a neuroanatomical tract-tracing study in the rat , 1999, Experimental Brain Research.

[70]  A. Graybiel The basal ganglia , 2000, Current Biology.

[71]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[72]  K. Nakano,et al.  Neural circuits and functional organization of the striatum , 2000, Journal of Neurology.

[73]  K. Nakano Neural circuits and topographic organization of the basal ganglia and related regions , 2000, Brain and Development.

[74]  B. G. Jenkins,et al.  Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks 1 1 Published on the World Wide Web on 28 August 2000. , 2000, Brain Research.

[75]  A. Parent,et al.  The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat , 2000, Neuroscience Research.

[76]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.

[77]  A. Loewy,et al.  Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat , 2000, The Journal of comparative neurology.

[78]  Anthony Dickinson,et al.  The 28th Bartlett Memorial Lecture Causal Learning: An Associative Analysis , 2001, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[79]  P Redgrave,et al.  Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat , 2001, The Journal of comparative neurology.

[80]  C. M. Thomson,et al.  Corticotectal and corticostriatal projections from the frontal eye fields of the cat: an anatomical examination using WGA-HRP. , 2001, Somatosensory & motor research.

[81]  Peter Redgrave,et al.  A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour , 2001, Biological Cybernetics.

[82]  Peter Redgrave,et al.  A computational model of action selection in the basal ganglia. I. A new functional anatomy , 2001, Biological Cybernetics.

[83]  M. Petrides,et al.  Wisconsin Card Sorting Revisited: Distinct Neural Circuits Participating in Different Stages of the Task Identified by Event-Related Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[84]  H. Miwa,et al.  Subthalamo-pallido-striatal axis: a feedback system in the basal ganglia , 2001, Neuroreport.

[85]  K. Mewes,et al.  The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. , 2001, Brain : a journal of neurology.

[86]  J. Dostrovsky,et al.  Synchronized Neuronal Discharge in the Basal Ganglia of Parkinsonian Patients Is Limited to Oscillatory Activity , 2002, The Journal of Neuroscience.

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

[88]  Karl J. Friston,et al.  Functional Anatomy of Visual Search: Regional Segregations within the Frontal Eye Fields and Effective Connectivity of the Superior Colliculus , 2002, NeuroImage.

[89]  M. Trimble,et al.  Abulia: A Delphi survey of British neurologists and psychiatrists , 2002, Movement disorders : official journal of the Movement Disorder Society.

[90]  A. Nambu,et al.  Functional significance of the cortico–subthalamo–pallidal ‘hyperdirect’ pathway , 2002, Neuroscience Research.

[91]  A. Loewy,et al.  Brainstem projections to midline and intralaminar thalamic nuclei of the rat , 2002, The Journal of comparative neurology.

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

[93]  S. Lehéricy,et al.  Foot, hand, face and eye representation in the human striatum. , 2003, Cerebral cortex.

[94]  T. Doubell,et al.  Functional Connectivity between the Superficial and Deeper Layers of the Superior Colliculus: An Anatomical Substrate for Sensorimotor Integration , 2003, The Journal of Neuroscience.

[95]  Walter Schneider,et al.  Controlled & automatic processing: behavior, theory, and biological mechanisms , 2003, Cogn. Sci..

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

[97]  S. Monsell Task switching , 2003, Trends in Cognitive Sciences.

[98]  Jose A Obeso,et al.  Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus , 2004, The European journal of neuroscience.

[99]  J. Tepper,et al.  Functional diversity and specificity of neostriatal interneurons , 2004, Current Opinion in Neurobiology.

[100]  M. Habib,et al.  Athymhormia and disorders of motivation in Basal Ganglia disease. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[101]  D. Willshaw,et al.  Models of the subthalamic nucleus. The importance of intranuclear connectivity. , 2004, Medical engineering & physics.

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

[103]  Minoru Hoshiyama,et al.  Hypokinesia of associated movement in Parkinson's disease: A symptom in early stages of the disease , 1994, Journal of Neurology.

[104]  S. Lehéricy,et al.  3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. , 2004, Cerebral cortex.

[105]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[106]  S. Clarke,et al.  Topography of cortico‐striatal connections in man: anatomical evidence for parallel organization , 2004, The European journal of neuroscience.

[107]  T. Robbins,et al.  Striatal contributions to working memory: a functional magnetic resonance imaging study in humans , 2004, The European journal of neuroscience.

[108]  K. Akert,et al.  Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey , 1978, Experimental Brain Research.

[109]  Jérôme Baufreton,et al.  Synaptic release of dopamine in the subthalamic nucleus , 2004, The European journal of neuroscience.

[110]  J. Paul Bolam,et al.  Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? , 2004, Trends in Neurosciences.

[111]  Andrew M. Poulos,et al.  The neuroscience of mammalian associative learning. , 2005, Annual review of psychology.

[112]  P. Delwaide,et al.  Functional changes of brainstem reflexes in Parkinson's disease conditioning of the blink reflex R2 component by paired and index finger stimulation , 2005, Journal of Neural Transmission.

[113]  G. Heit,et al.  Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels , 2005, Brain Research Reviews.

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

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

[116]  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.

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

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

[119]  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.

[120]  M. Petrides,et al.  Functional role of the basal ganglia in the planning and execution of actions , 2006, Annals of neurology.

[121]  Mark D. Humphries,et al.  A robot model of the basal ganglia: Behavior and intrinsic processing , 2006, Neural Networks.

[122]  P. Redgrave,et al.  The short-latency dopamine signal: a role in discovering novel actions? , 2006, Nature Reviews Neuroscience.

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

[124]  K. Gurney,et al.  A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia , 2006, The Journal of Neuroscience.

[125]  Thomas Wichmann,et al.  Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. , 2006, Journal of neurophysiology.

[126]  W. Schultz Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

[127]  P. Dayan,et al.  Tonic dopamine: opportunity costs and the control of response vigor , 2007, Psychopharmacology.

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

[129]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[130]  H. Kita Globus pallidus external segment. , 2007, Progress in brain research.

[131]  A. Parent,et al.  The microcircuitry of primate subthalamic nucleus. , 2007, Parkinsonism & related disorders.

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

[133]  Thomas Wichmann,et al.  Circuits and circuit disorders of the basal ganglia. , 2007, Archives of neurology.

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

[135]  A. Björklund,et al.  Dopamine neuron systems in the brain: an update , 2007, Trends in Neurosciences.

[136]  J. Tepper,et al.  GABA and the basal ganglia : from molecules to systems , 2007 .

[137]  Peter Brown,et al.  Paradoxes of functional neurosurgery: Clues from basal ganglia recordings , 2008, Movement disorders : official journal of the Movement Disorder Society.

[138]  P. Redgrave,et al.  What is reinforced by phasic dopamine signals? , 2008, Brain Research Reviews.

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

[140]  J. Doyon Motor sequence learning and movement disorders , 2008, Current opinion in neurology.

[141]  Richard S. J. Frackowiak,et al.  Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia , 2008, The Journal of Neuroscience.

[142]  Yasuyuki Okuma,et al.  The clinical spectrum of freezing of gait in Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[143]  M. Hallett The intrinsic and extrinsic aspects of freezing of gait , 2008, Movement disorders : official journal of the Movement Disorder Society.

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

[145]  Kaoru Takakusaki,et al.  Neurobiological Basis of Controlling Posture and Locomotion , 2008, Adv. Robotics.

[146]  Suzanne N Haber,et al.  Low-Pass Filter Properties of Basal Ganglia–Cortical–Muscle Loops in the Normal and MPTP Primate Model of Parkinsonism , 2008, The Journal of Neuroscience.

[147]  J. Obeso,et al.  The basal ganglia in Parkinson's disease: Current concepts and unexplained observations , 2008, Annals of neurology.

[148]  S. Fahn The history of dopamine and levodopa in the treatment of Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

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

[150]  Pietro Mazzoni,et al.  Parallel Explicit and Implicit Control of Reaching , 2009, PloS one.

[151]  D. Brooks,et al.  Imaging neurodegeneration in Parkinson's disease. , 2009, Biochimica et biophysica acta.

[152]  J. Horvitz Stimulus–response and response–outcome learning mechanisms in the striatum , 2009, Behavioural Brain Research.

[153]  F. Fujiyama,et al.  Single Nigrostriatal Dopaminergic Neurons Form Widely Spread and Highly Dense Axonal Arborizations in the Neostriatum , 2009, The Journal of Neuroscience.

[154]  A. Strafella,et al.  L-Dopa Medication in Parkinson's Disease Restores Activity in the Motor Cortico-Striatal Loop but Does Not Modify the Cognitive Network , 2009, PloS one.

[155]  B. Day,et al.  What can man do without basal ganglia motor output? The effect of combined unilateral subthalamotomy and pallidotomy in a patient with Parkinson's disease , 2009, Experimental Neurology.

[156]  R. Palmiter,et al.  Restriction of dopamine signaling to the dorsolateral striatum is sufficient for many cognitive behaviors , 2009, Proceedings of the National Academy of Sciences.

[157]  Erwan Bezard,et al.  Chronic dopaminergic stimulation in Parkinson's disease: from dyskinesias to impulse control disorders , 2009, The Lancet Neurology.

[158]  Peter Redgrave,et al.  Short-Latency Visual Input to the Subthalamic Nucleus Is Provided by the Midbrain Superior Colliculus , 2009, The Journal of Neuroscience.

[159]  Jean-Michel Deniau,et al.  Striatal Medium-Sized Spiny Neurons: Identification by Nuclear Staining and Study of Neuronal Subpopulations in BAC Transgenic Mice , 2009, PloS one.

[160]  V. Mark,et al.  SUBTHALAMIC NUCLEUS AND ITS CONNECTIONS: ANATOMIC SUBSTRATE FOR THE NETWORK EFFECTS OF DEEP BRAIN STIMULATION , 2009, Neurology.

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

[162]  R. Costa,et al.  Chronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making , 2009, Science.

[163]  A. Compston Progressive lenticular degeneration: a familial nervous disease associated with cirrhosis of the liver, by S. A. Kinnier Wilson, (From the National Hospital, and the Laboratory of the National Hospital, Queen Square, London) Brain 1912: 34; 295-509. , 2009, Brain : a journal of neurology.

[164]  Lynn Rochester,et al.  Motor learning in Parkinson's disease: limitations and potential for rehabilitation. , 2009, Parkinsonism & related disorders.

[165]  E. Bézard,et al.  Initial clinical manifestations of Parkinson's disease: features and pathophysiological mechanisms , 2009, The Lancet Neurology.

[166]  V. Sossi,et al.  Longitudinal progression of sporadic Parkinson's disease: a multi-tracer positron emission tomography study. , 2009, Brain : a journal of neurology.

[167]  D. Aarsland,et al.  Occurrence and risk factors for apathy in Parkinson disease: a 4-year prospective longitudinal study , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[168]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

[169]  Gadi Goelman,et al.  Evidence for asymmetric intra substantia nigra functional connectivity—application to basal ganglia processing , 2010, NeuroImage.

[170]  M. Delong,et al.  Changing Views of Basal Ganglia Circuits and Circuit Disorders , 2010, Clinical EEG and neuroscience.

[171]  B. Knowlton,et al.  Concurrent discrimination learning in Parkinson's disease. , 2010, Behavioral neuroscience.

[172]  Lars Schwabe,et al.  Memory formation under stress: Quantity and quality , 2010, Neuroscience & Biobehavioral Reviews.

[173]  Jorge Iriarte,et al.  Coupling between Beta and High-Frequency Activity in the Human Subthalamic Nucleus May Be a Pathophysiological Mechanism in Parkinson's Disease , 2010, The Journal of Neuroscience.

[174]  B. Balleine,et al.  Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action , 2010, Neuropsychopharmacology.

[175]  Bogdan Draganski,et al.  Brain structure in movement disorders: a neuroimaging perspective. , 2010, Current opinion in neurology.

[176]  Tao Wu,et al.  Effective connectivity of neural networks in automatic movements in Parkinson's disease , 2010, NeuroImage.

[177]  John S. McKenzie,et al.  The Basal Ganglia Iv: New Ideas And Data On Structure And Function , 2011 .

[178]  Roshan Cools,et al.  Habitual versus Goal-directed Action Control in Parkinson Disease , 2011, Journal of Cognitive Neuroscience.