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

• Ferrier, D. The Functions of the Brain (Putnam's Sons, New York, 1876).
  Book Google Scholar
• Penney, J. B. Jr & Young, A. B. Striatal inhomogeneities and basal ganglia function. Mov. Disord. 1, 3–15 (1986).
  Article PubMed Google Scholar
• Albin, R. L., Young, A. B. & Penney, J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366–375 (1989).
  Article CAS PubMed Google Scholar
• Chevalier, G. & Deniau, J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 13, 277–281 (1990). This review introduced a conceptual development in suggesting that a pause in neuronal firing in basal ganglia output nuclei disinhibits efferent targets and is the major physiological mechanism by which the basal ganglia exert their effects on behaviour.
  Article CAS PubMed Google Scholar
• Gerfen, C. R. & Wilson, C. J. in Handbook of Chemical Neuroanatomy Vol 12 (eds Swanson, L. W., Bjorklund, A. & Hokfelt, T.) 371–468 (Elsevier, Amsterdam, 1996).
  Google Scholar
• DeLong, M. R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281–285 (1990). A classic review of the basal ganglia pathophyisiological model and the concepts on which it is based.
  Article CAS PubMed Google Scholar
• Gerfen, C. R. et al. D1 and D2 dopamine receptor regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429–1431 (1990).
  Article CAS PubMed Google Scholar
• Crossman, A. R. Primate models of dyskinesia: the experimental approach to the study of basal ganglia-related involuntary movement disorders. Neuroscience 21, 1–40 (1987).
  Article CAS PubMed Google Scholar
• Bevan, M. D., Bolam, J. P. & Crossman, A. R. Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Eur. J. Neurosci. 6, 320–334 (1994).
  Article CAS PubMed Google Scholar
• Redgrave, P. Basal ganglia. Scholarpedia 2, 1825 (2007).
  Article Google Scholar
• Wu, Y., Richard, S. & Parent, A. The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci. Res. 38, 49–62 (2000).
  Article CAS PubMed Google Scholar
• Matamales, M. et al. Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS ONE 4, e4770 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Hartmann-von Monakow, K. H., Akert, K. & Kunzle, H. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. 33, 395–403 (1978).
  Google Scholar
• Nambu, A., Tokuno, H. & Takada, M. Functional significance of the cortico–subthalamo–pallidal 'hyperdirect' pathway. Neurosci. Res. 43, 111–117 (2002).
  Article PubMed Google Scholar
• Lanciego, J. L. et al. Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus. Eur. J. Neurosci. 19, 1267–1277 (2004).
  Article PubMed Google Scholar
• Feger, J., Bevan, M. & Crossman, A. R. 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. Neuroscience 60, 125–132 (1994).
  Article CAS PubMed Google Scholar
• Coizet, V. et al. Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J. Neurosci. 29, 5701–5709 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Mena-Segovia, J., Bolam, J. P. & Magill, P. J. Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci. 27, 585–588 (2004).
  Article CAS PubMed Google Scholar
• Smith, Y., Bevan, M. D., Shink, E. & Bolam, J. P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86, 353–387 (1998).
  Article CAS PubMed Google Scholar
• Miwa, H., Fuwa, T., Nishi, K. & Kondo, T. Subthalamo-pallido-striatal axis: a feedback system in the basal ganglia. Neuroreport 12, 3795–3798 (2001).
  Article CAS PubMed Google Scholar
• Shink, E., Bevan, M. D., Bolam, J. P. & Smith, Y. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 73, 335–357 (1996).
  Article CAS PubMed Google Scholar
• Kita, H. in Gaba And The Basal Ganglia: From Molecules To Systems (eds Tepper, J., Absercrombie, E. & Bolam, J. P.) 111–133 (Elsevier, Amsterdam, 2007).
  Book Google Scholar
• Bevan, M. D., Booth, P. A. C., Eaton, S. A. & Bolam, J. P. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J. Neurosci. 18, 9438–9452 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kita, H., Tokuno, H. & Nambu, A. Monkey globus pallidus external segment neurons projecting to the neostriatum. Neuroreport 10, 1467–1472 (1999).
  Article CAS PubMed Google Scholar
• McGeorge, A. J. & Faull, R. L. M. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503–537 (1989).
  Article CAS PubMed Google Scholar
• Romanelli, P., Esposito, V., Schaal, D. W. & Heit, G. Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels. Brain Res. Rev. 48, 112–128 (2005).
  Article PubMed Google Scholar
• Wiesendanger, E., Clarke, S., Kraftsik, R. & Tardif, E. Topography of cortico-striatal connections in man: anatomical evidence for parallel organization. Eur. J. Neurosci. 20, 1915–1922 (2004).
  Article CAS PubMed Google Scholar
• Nakano, K., Kayahara, T., Tsutsumi, T. & Ushiro, H. Neural circuits and functional organization of the striatum. J. Neurol. 247, V1–V15 (2000).
  Article PubMed Google Scholar
• Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann. Rev. Neurosci. 9, 357–381 (1986). The classic and first description of the re-entrant looped architecture by which the basal ganglia interact with external structures.
  Article CAS PubMed Google Scholar
• McHaffie, J. G., Stanford, T. R., Stein, B. E., Coizet, V. & Redgrave, P. Subcortical loops through the basal ganglia. Trends Neurosci. 28, 401–407 (2005).
  Article CAS PubMed Google Scholar
• Bolam, J. P. & Bennett, B. D. in Molecular and Cellular Mechanims of Neostriatal Function (eds Ariano, M. A. & Surmeier, D. J.) 1–19 (R. G. Landes Co., Texas, 1995).
  Google Scholar
• Gillies, A. & Willshaw, D. Models of the subthalamic nucleus: the importance of intranuclear connectivity. Med. Eng. Phys. 26, 723–732 (2004).
  Article CAS PubMed Google Scholar
• Benarroch, E. E. Subthalamic nucleus and its connections: anatomic substrate for the network effects of deep brain stimulation. Neurology 70, 1991–1995 (2008).
  Article PubMed Google Scholar
• Parent, M. & Parent, A. The microcircuitry of primate subthalamic nucleus. Parkinsonism Relat. Disord. 13, S292–S295 (2007).
  Article PubMed Google Scholar
• Nakano, K. Neural circuits and topographic organization of the basal ganglia and related regions. Brain Dev. 22, S5–S16 (2000).
  Article PubMed Google Scholar
• Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W. & Pennartz, C. M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468–474 (2004).
  Article CAS PubMed Google Scholar
• Draganski, B. et al. Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J. Neurosci. 28, 7143–7152 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Lehericy, S. et al. 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb. Cortex 14, 1302–1309 (2004).
  Article PubMed Google Scholar
• Doron, O. & Goelman, G. Evidence for asymmetric intra substantia nigra functional connectivity-application to basal ganglia processing. Neuroimage 49, 2940–2946 (2010).
  Article PubMed Google Scholar
• Krout, K. E., Belzer, R. E. & Loewy, A. D. Brainstem projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 448, 53–101 (2002).
  Article PubMed Google Scholar
• Krout, K. E., Loewy, A. D., Westby, G. W. M. & Redgrave, P. Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 431, 198–216 (2001).
  Article CAS PubMed Google Scholar
• Krout, K. E. & Loewy, A. D. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol. 424, 111–141 (2000).
  Article CAS PubMed Google Scholar
• Erro, E., Lanciego, J. L. & Gimenez-Amaya, J. M. Relationships between thalamostriatal neurons and pedunculopontine projections to the thalamus: a neuroanatomical tract-tracing study in the rat. Exp. Brain Res. 127, 162–170 (1999).
  Article CAS PubMed Google Scholar
• Bjorklund, A. & Dunnett, S. B. Dopamine neuron systems in the brain: an update. Trends Neurosci. 30, 194–202 (2007).
  Article PubMed CAS Google Scholar
• Matsuda, W. et al. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 29, 444–453 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Smith, Y., Lavoie, B., Dumas, J. & Parent, A. Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey. Brain Res. 482, 381–386 (1989).
  Article CAS PubMed Google Scholar
• Cragg, S. J., Baufreton, J., Xue, Y., Bolam, J. P. & Bevan, M. D. Synaptic release of dopamine in the subthalamic nucleus. Eur. J. Neurosci. 20, 1788–1802 (2004).
  Article PubMed Google Scholar
• Grace, A. A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41, 1–24 (1991).
  Article CAS PubMed Google Scholar
• Redgrave, P., Prescott, T. & Gurney, K. N. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89, 1009–1023 (1999). A general description of the mechanisms and computational requirements of selection performed by the basal ganglia.
  Article CAS PubMed Google Scholar
• Mink, J. W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381–425 (1996).
  Article CAS PubMed Google Scholar
• Hikosaka, O., Takikawa, Y. & Kawagoe, R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80, 953–978 (2000).
  Article CAS PubMed Google Scholar
• Redgrave, P. & Gurney, K. The short-latency dopamine signal: a role in discovering novel actions? Nature Rev. Neurosci. 7, 967–975 (2006).
  Article CAS Google Scholar
• Redgrave, P., Gurney, K. & Reynolds, J. What is reinforced by phasic dopamine signals? Brain Res. Rev. 58, 322–339 (2008).
  Article CAS PubMed Google Scholar
• Schultz, W. Behavioral theories and the neurophysiology of reward. Annu. Rev. Psychol. 57, 87–115 (2006).
  Article PubMed Google Scholar
• Alexander, G. E. & DeLong, M. R. Microstimulation of the primate neurostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. J. Neurophysiol. 53, 1417–1430 (1985).
  Article CAS PubMed Google Scholar
• Kimura, M. Behaviorally contingent property of movement-related activity of the primate putamen. J. Neurophysiol. 63, 1277–1296 (1990).
  Article CAS PubMed Google Scholar
• Flaherty, A. W. & Graybiel, A. M. Two input systems for body representation in the primate striatal matrix: experimental evidence in the squirrel monkey. J. Neurosci. 13, 1120–1137 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Hikosaka, O., Sakamoto, M. & Usui, S. Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. J. Neurophysiol. 61, 780–798 (1989).
  Article CAS PubMed Google Scholar
• Hikosaka, O., Sakamoto, M. & Usui, S. Functional properties of monkey caudate neurons II. Visual and auditory responses. J. Neurophysiol. 61, 799–813 (1989).
  Article CAS PubMed Google Scholar
• Tremblay, L., Hollerman, J. R. & Schultz, W. Modifications of reward expectation-related neuronal activity during learning in primate striatum. J. Neurophysiol. 80, 964–977 (1998).
  Article CAS PubMed Google Scholar
• Scholz, V. H. et al. Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks. Brain Res. 879, 204–215 (2000).
  Article CAS PubMed Google Scholar
• Gerardin, E. et al. Foot, hand, face and eye representation in the human striatum. Cereb. Cortex 13, 162–169 (2003).
  Article PubMed Google Scholar
• Dickinson, A. The 28th Bartlett Memorial Lecture Causal learning: an associative analysis. Q. J. Exp. Psychol. B. 54, 3–25 (2001).
  Article CAS PubMed Google Scholar
• Balleine, B. W., Lijeholm, M. & Ostlund, S. B. The integrative function of the basal ganglia in instrumental conditioning. Behav. Brain Res. 199, 43–52 (2009).
  Article PubMed Google Scholar
• Balleine, B. W. & O'Doherty, J. P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35, 48–69 (2009). This paper provides well-written and clearly explained views about the role of the basal ganglia in the control of human and rodent behaviour.
  Article PubMed Central Google Scholar
• Yin, H. H. & Knowlton, B. J. The role of the basal ganglia in habit formation. Nature Rev. Neurosci. 7, 464–476 (2006). An excellent review of the role of the basal ganglia in habitual and goal-directed control.
  Article CAS Google Scholar
• Thorndike, E. L. Animal Intelligence. (Macmillan, New York, 1911).
  Google Scholar
• Spence, K. W. Behavior Theory and Conditioning (Yale Univ. Press, New Haven, 1956).
  Book Google Scholar
• Dickinson, A. & Balleine, B. Motivational control of goal-directed action. Anim. Learn. Behav. 22, 1–18 (1994).
  Article Google Scholar
• Adams, C. D. & Dickinson, A. Instrumental responding following reinforcer devaluation. Q. J. Exp. Psychol. 33, 109–121 (1981).
  Article Google Scholar
• Hammond, L. J. The effect of contingency upon the appetitive conditioning of free-operant behavior. J. Exp. Anal. Behav. 34, 297–304 (1980).
  Article CAS PubMed PubMed Central Google Scholar
• Balleine, B. W. & Dickinson, A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37, 407–419 (1998).
  Article CAS PubMed Google Scholar
• Horvitz, J. C. Stimulus-response and response-outcome learning mechanisms in the striatum. Behav. Brain Res. 199, 129–140 (2009).
  Article PubMed Google Scholar
• Schwabe, L., Wolf, O. T. & Oitzl, M. S. Memory formation under stress: quantity and quality. Neurosci. Biobehav. Rev. 34, 584–591 (2010).
  Article PubMed Google Scholar
• Hikosaka, O. & Isoda, M. Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms. Trends Cogn. Sci. 14, 154–161 (2010). An important recent analysis of the neural mechanisms responsible for switching between automatic and controlled behaviour.
  Article PubMed PubMed Central Google Scholar
• Monsell, S. Task switching. Trends Cogn. Sci. 7, 134–140 (2003).
  Article PubMed Google Scholar
• Dickinson, A., Nicholas, D. J. & Adams, C. D. The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q. J. Exp. Psychol. 35, 35–51 (1983).
  Article Google Scholar
• Heuer, H., Spijkers, W., Kiesswetter, E. & Schmidtke, V. Effects of sleep loss, time of day, and extended mental work on implicit and explicit learning of sequences. J. Exp. Psychol. Appl. 4, 139–162 (1998).
  Article CAS PubMed Google Scholar
• Dias-Ferreira, E. et al. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325, 621–625 (2009).
  Article CAS PubMed Google Scholar
• Mazzoni, P. & Wexler, N. S. Parallel explicit and implicit control of reaching. PLoS ONE 4, e7557 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Balleine, B. W. & Ostlund, S. B. Still at the choice-point: action selection and initiation in istrumental conditioning. encoding. Ann. NY Acad. Sci. 1104, 147–171 (2007).
  Article PubMed Google Scholar
• Daw, N. D., Niv, Y. & Dayan, P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nature Neurosci. 8, 1704–1711 (2005).
  Article CAS PubMed Google Scholar
• Schneider, W. & Chein, J. M. Controlled & automatic processing: behavior, theory, and biological mechanisms. Cogn. Sci. 27, 525–559 (2003). An excellent review of the differences between controlled and automatic processing in humans.
  Article Google Scholar
• Yin, H. H., Knowlton, B. J. & Balleine, B. W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 19, 181–189 (2004).
  Article PubMed Google Scholar
• Yin, H. H., Knowlton, B. J. & Balleine, B. W. Blockade of NMDA receptors in the dorsomedial striatum prevents action–outcome learning in instrumental conditioning. Eur. J. Neurosci. 22, 505–512 (2005).
  Article PubMed Google Scholar
• Yin, H. H., Ostlund, S. B., Knowlton, B. J. & Balleine, B. W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513–523 (2005).
  Article PubMed Google Scholar
• Yin, H. H., Knowlton, B. J. & Balleine, B. W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning. Behav. Brain Res. 166, 189–196 (2006).
  Article PubMed Google Scholar
• Miyachi, S., Hikosaka, O., Miyashita, K., Karadi, Z. & Rand, M. K. Differential roles of monkey striatum in learning of sequential hand movement. Exp. Brain Res. 115, 1–5 (1997).
  Article CAS PubMed Google Scholar
• Miyachi, S., Hikosaka, O. & Lu, X. F. Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp. Brain Res. 146, 122–126 (2002).
  Article PubMed Google Scholar
• Monchi, O., Petrides, M., Petre, V., Worsley, K. & Dagher, A. Wisconsin Card Sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. J. Neurosci. 21, 7733–7741 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Monchi, O., Petrides, M., Strafella, A. P., Worsley, K. J. & Doyon, J. Functional role of the basal ganglia in the planning and execution of actions. Ann. Neurol. 59, 257–264 (2006).
  Article PubMed Google Scholar
• Lewis, S. J. G., Dove, A., Robbins, T. W., Barker, R. A. & Owen, A. M. Striatal contributions to working memory: a functional magnetic resonance imaging study in humans. Eur. J. Neurosci. 19, 755–760 (2004).
  Article PubMed Google Scholar
• Jueptner, M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. & Passingham, R. E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 77, 1325–1337 (1997).
  Article CAS PubMed Google Scholar
• Lehericy, S. et al. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc. Natl Acad. Sci.USA 102, 12566–12571 (2005). An early study in humans indicating that different striatal regions become engaged during different phases of motor learning.
  Article CAS PubMed PubMed Central Google Scholar
• Tanaka, S. C., Balleine, B. W. & O'Doherty, J. P. Calculating consequences: brain systems that encode the causal effects of actions. J. Neurosci. 28, 6750–6755 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Tricomi, E., Balleine, B. W. & O'Doherty, J. P. A specific role for posterior dorsolateral striatum in human habit learning. Eur. J. Neurosci. 29, 2225–2232 (2009).
  Article PubMed PubMed Central Google Scholar
• Gurney, K., Prescott, T. J. & Redgrave, P. A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol. Cybern. 84, 401–410 (2001).
  Article CAS PubMed Google Scholar
• Gurney, K., Prescott, T. J. & Redgrave, P. A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour. Biol. Cybern. 84, 411–423 (2001).
  Article CAS PubMed Google Scholar
• Humphries, M. D., Stewart, R. D. & Gurney, K. N. A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. 26, 12921–12942 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Prescott, T. J., Gonzalez, F. M. M., Gurney, K., Humphries, M. D. & Redgrave, P. A robot model of the basal ganglia: behavior and intrinsic processing. Neural Netw. 19, 31–61 (2006).
  Article PubMed Google Scholar
• Singh, S. P., Barto, A. G. & Chentanez, N. in Advances in Neural Information Processing Systems (eds Saul, L. K., Weiss, H. & Bottou, L.) 1281–1288 (MIT Press, Cambridge, Massachusetts, 2005).
  Google Scholar
• Doubell, T. P., Skaliora, I., Baron, J. & King, A. J. Functional connectivity between the superficial and deeper layers of the superior colliculus: an anatomical substrate for sensorimotor integration. J. Neurosci. 23, 6596–6607 (2003).
  Article PubMed PubMed Central Google Scholar
• Sommer, M. A. & Wurtz, R. H. Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J. Neurophysiol. 83, 1979–2001 (2000).
  Article CAS PubMed Google Scholar
• McHaffie, J. G., Thomson, C. M. & Stein, B. E. Corticotectal and corticostriatal projections from the frontal eye fields of the cat: an anatomical examination using WGA-HRP. Somatosens Mot. Res. 18, 117–130 (2001).
  Article CAS PubMed Google Scholar
• Gitelman, D. R., Parrish, T. B., Friston, K. J. & Mesulam, M. M. Functional anatomy of visual search: regional segregations within the frontal eye fields and effective connectivity of the superior colliculus. Neuroimage 15, 970–982 (2002).
  Article PubMed Google Scholar
• Takakusaki, K. & Okumura, T. Neurobiological basis of controlling posture and locomotion. Adv. Robot. 22, 1629–1663 (2008).
  Article Google Scholar
• Pavese, N. & Brooks, D. J. Imaging neurodegeneration in Parkinson's disease. Biochim. Biophys. Acta 1792, 722–729 (2009).
  Article CAS PubMed Google Scholar
• Morrish, P. K., Sawle, G. V. & Brooks, D. J. Clinical and [18F] dopa PET findings in early Parkinson's disease. J. Neurol. Neurosurg. Psychiatr. 59, 597–600 (1995).
  Article CAS Google Scholar
• Kish, S. J., Shannak, K. & Hornykiewicz, O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N. Engl. J. Med. 318, 876–880 (1988). A key paper indicating a differential loss of dopamine from the sensorimotor territories of the caudal putamen in patients with Parkinson's disease.
  Article CAS PubMed Google Scholar
• Fearnley, J. M. & Lees, A. J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114, 2283–2301 (1991).
  Article PubMed Google Scholar
• Marsden, C. D. The mysterious motor function of the basal ganglia: the Robert Wartenberg Lecture. Neurology 32, 514–539 (1982). Classic, fundamental appraisal of the origin of movement disorders in early Parkinson's disease.
  Article CAS PubMed Google Scholar
• Rodriguez-Oroz, M. C. et al. Initial clinical manifestations of Parkinson's disease: features and pathophysiological mechanisms. Lancet Neurol. 8, 1128–1139 (2009).
  Article CAS PubMed Google Scholar
• Schwab, R. S., Chafetz, M. E. & Walker, S. Control of two simultaneous voluntary motor acts in normals and in parkinsonism. AMA Arch. Neurol. Psychiatry 72, 591–598 (1954).
  Article CAS PubMed Google Scholar
• Hoshiyama, M., Kaneoke, Y., Koike, Y., Takahashi, A. & Watanabe, S. Hypokinesia of associated movement in Parkinson's disease: a symptom in early stages of the disease. J. Neurol. 241, 517–521 (1994).
  Article CAS PubMed Google Scholar
• Knowlton, B. J., Mangels, J. A. & Squire, L. R. A neostriatal habit learning system in humans. Science 273, 1399–1402 (1996).
  Article CAS PubMed Google Scholar
• Hallett, M. The intrinsic and extrinsic aspects of freezing of gait. Mov. Disord. 23, S439–S443 (2008).
  Article PubMed PubMed Central Google Scholar
• Wu, T., Chan, P. & Hallett, M. Effective connectivity of neural networks in automatic movements in Parkinson's disease. Neuroimage 49, 2581–2587 (2010).
  Article CAS PubMed Google Scholar
• Moody, T. D., Chang, G. Y., Vanek, Z. F. & Knowlton, B. J. Concurrent discrimination learning in Parkinson's disease. Behav. Neurosci. 124, 1–8 (2010).
  Article PubMed Google Scholar
• Faure, A., Haberland, U., Conde, F. & El Massioui, N. Lesion to the nigrostriatal dopamine system disrupts stimulus- response habit formation. J. Neurosci. 25, 2771–2780 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Benecke, R., Rothwell, J. C., Dick, J. P., Day, B. L. & Marsden, C. D. Performance of simultaneous movements in patients with Parkinson's disease. Brain 109, 739–757 (1986).
  Article PubMed Google Scholar
• Nieuwboer, A., Rochester, L., Muncks, L. & Swinnen, S. P. Motor learning in Parkinson's disease: limitations and potential for rehabilitation. Parkinsonism Relat. Disord. 15, S53–S58 (2009).
  Article PubMed Google Scholar
• Okuma, Y. & Yanagisawa, N. The clinical spectrum of freezing of gait in Parkinson's disease. Mov. Disord. 23, S426–S430 (2008).
  Article PubMed Google Scholar
• Benecke, R., Rothwell, J. C., Dick, J. P., Day, B. L. & Marsden, C. D. Disturbance of sequential movements in patients with Parkinson's disease. Brain 110, 361–379 (1987).
  Article PubMed Google Scholar
• Stelmach, G. E., Worringham, C. J. & Strand, E. A. Movement preparation in Parkinson's disease. The use of advance information. Brain 109, 1179–1194 (1986).
  Article PubMed Google Scholar
• Doyon, J. Motor sequence learning and movement disorders. Curr. Opin. Neurol. 21, 478–483 (2008).
  Article PubMed Google Scholar
• Nandhagopal, R. et al. Longitudinal progression of sporadic Parkinson's disease: a multi-tracer positron emission tomography study. Brain 132, 2970–2979 (2009).
  Article CAS PubMed Google Scholar
• Rogers, M. A., Phillips, J. G., Bradshaw, J. L., Iansek, R. & Jones, D. Provision of external cues and movement sequencing in Parkinson's disease. Motor Control 2, 125–132 (1998).
  Article CAS PubMed Google Scholar
• Jahanshahi, M., Brown, R. G. & Marsden, C. D. Simple and choice reaction time and the use of advance information for motor preparation in Parkinson's disease. Brain 115, 539–564 (1992).
  Article PubMed Google Scholar
• Mesulam, M. M. From sensation to cognition. Brain 121, 1013–1052 (1998).
  Article PubMed Google Scholar
• Lozza, A., Pepin, J. L., Rapisarda, G., Moglia, A. & Delwaide, P. J. Functional changes of brainstem reflexes in Parkinson's disease. Conditioning of the blink reflex R2 component by paired and index finger stimulation. J. Neural Transm. 104, 679–687 (1997).
  Article CAS PubMed Google Scholar
• Fanselow, M. S. & Poulos, A. M. The neuroscience of mammalian associative learning. Annu. Rev. Psychol. 56, 207–234 (2005).
  Article PubMed Google Scholar
• Cardinal, R. N., Parkinson, J. A., Hall, J. & Everitt, B. J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352 (2002).
  Article PubMed Google Scholar
• DeLong, M. R. & Wichmann, T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 64, 20–24 (2007).
  Article PubMed Google Scholar
• Obeso, J. A. et al. The basal ganglia in Parkinson's disease: current concepts and unexplained observations. Ann. Neurol. 64, S30–S46 (2008).
  Article PubMed Google Scholar
• Filion, M. & Tremblay, L. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res. 547, 142–151 (1991).
  CAS PubMed Google Scholar
• Rodriguez-Oroz, M. C. et al. The subthalamic nucleus in Parkinson's disease: somatotopic organization and physiological characteristics. Brain 124, 1777–1790 (2001).
  Article CAS PubMed Google Scholar
• Levy, R., Hutchison, W. D., Lozano, A. M. & Dostrovsky, J. O. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J. Neurosci. 22, 2855–2861 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Wichmann, T. & Soares, J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J. Neurophysiol. 95, 2120–2133 (2006).
  Article PubMed CAS Google Scholar
• Lopez-Azcarate, J. et al. Coupling between β and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson's disease. J. Neurosci. 30, 6667–6677 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Brown, P. & Marsden, C. D. What do the basal ganglia do? Lancet 351, 1801–1804 (1998).
  Article CAS PubMed Google Scholar
• Hallett, M. & Khoshbin, S. A physiological mechanism of bradykinesia. Brain 103, 301–314 (1980).
  Article CAS PubMed Google Scholar
• Marsden, C. D. & Obeso, J. A. The function of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain 117, 877–897 (1994). A classic approach to the enigma of how the basal ganglia output can be destroyed without deteriorating the movement further in patients with Parkinson's disease.
  Article PubMed Google Scholar
• Rivlin-Etzion, M. et al. Low-pass filter properties of basal ganglia-cortical-muscle loops in the normal and MPTP primate model of parkinsonism. J. Neurosci. 28, 633–649 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Brown, P. & Eusebio, A. Paradoxes of functional neurosurgery: clues from basal ganglia recordings. Mov. Disord. 23, 12–20 (2008).
  Article PubMed Google Scholar
• Vitek, J. L. et al. Microelectrode-guided pallidotomy: technical approach and its application in medically intractable Parkinson's disease. J. Neurosurg. 88, 1027–1043 (1998).
  Article CAS PubMed Google Scholar
• Vijayaraghavan, L., Krishnamoorthy, E. S., Brown, R. G. & Trimble, M. R. Abulia: a delphi survey of British neurologists and psychiatrists. Mov. Disord. 17, 1052–1057 (2002).
  Article PubMed Google Scholar
• Habib, M. Athymhormia and disorders of motivation in Basal Ganglia disease. J. Neuropsychiatry Clin. Neurosci. 16, 509–524 (2004).
  Article PubMed Google Scholar
• Pedersen, K. F., Alves, G., Aarsland, D. & Larsen, J. P. Occurrence and risk factors for apathy in Parkinson disease: a 4-year prospective longitudinal study. J. Neurol. Neurosurg. Psychiatr. 80, 1279–1282 (2009).
  Article CAS Google Scholar
• Voon, V. et al. Chronic dopaminergic stimulation in Parkinson's disease: from dyskinesias to impulse control disorders. Lancet Neurol. 8, 1140–1149 (2009).
  Article CAS PubMed Google Scholar
• Niv, Y., Daw, N. D., Joel, D. & Dayan, P. Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology (Berlin) 191, 507–520 (2007).
  Article CAS Google Scholar
• Tepper, J. M. & Bolam, J. P. Functional diversity and specificity of neostriatal interneurons. Curr. Opin. Neurobiol. 14, 685–692 (2004).
  Article CAS PubMed Google Scholar
• Bergman, H., Wichmann, T., Karmon, B. & DeLong, M. R. in The Basal Ganglia IV: New Ideas and Data on Structure and Function (eds Percheron, G., McKenzie, J. S. & Feger, J.) 317–325 (Plenum Press, New York, 1994).
  Book Google Scholar
• Darvas, M. & Palmiter, R. D. Restriction of dopamine signaling to the dorsolateral striatum is sufficient for many cognitive behaviors. Proc. Natl Acad. Sci. USA 106, 14664–14669 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Jubault, T., Monetta, L., Strafella, A. P., Lafontaine, A. L. & Monchi, O. L-dopa medication in Parkinson's disease restores activity in the motor cortico-striatal loop but does not modify the cognitive network. PLoS ONE 4, e6154 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Obeso, J. A. 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. Exp. Neurol. 220, 283–292 (2009).
  Article CAS PubMed Google Scholar
• de Wit, S., Barker, R. A., Dickinson, A. D. & Cools, R. Habitual versus goal-directed action control in Parkinson disease. J. Cogn. Neurosci. 30 Apr 2010 (doi: 10.1162/jocn.2010.21514).
  Article PubMed Google Scholar
• Graybiel, A. M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359–387 (2008). An excellent review of habitual behaviour.
  Article CAS PubMed Google Scholar
• DeLong, M. & Wichmann, T. Changing views of basal ganglia circuits and circuit disorders. Clin. EEG Neurosci. 41, 61–67 (2010).
  Article PubMed PubMed Central Google Scholar
• Draganski, B. & Bhatia, K. P. Brain structure in movement disorders: a neuroimaging perspective. Curr. Opin. Neurol. 23, 413–419 (2010).
  Article PubMed Google Scholar
• Wilson, S. A. K. Progressive lenticular degeneratio. A familial nervous disease associated with cirrhosis of the liver. Brain 34, 295–507 (1912).
  Article Google Scholar
• Wilson, S. A. K. Disorders of motility and tone. Lancet Neurol. 1, 1–103 (1925).
  Google Scholar
• Purdon Martin, J. Hemichorea resulting from a local lesion of the brain. (The syndrome of the body of Luys). Brain 50, 637–651 (1927).
  Article Google Scholar
• Purdon Martin, J. & Alcock, N. S. Hemichorea associated with a lesion of the corput Luysii. Brain 57, 504–516 (1934).
  Article Google Scholar
• Denny-Brown, D. The Basal Ganglia (Oxford Univ. Press, Oxford, 1962).
  Google Scholar
• Carpenter, M. B., Whittier, J. R. & Mettler, F. A. Analysis of choreoid hyperkinesia in the Rhesus monkey; surgical and pharmacological analysis of hyperkinesia resulting from lesions in the subthalamic nucleus of Luys. J. Comp. Neurol. 92, 293–331 (1950).
  Article CAS PubMed Google Scholar
• Martin, J. P. & McCaul, I. R. Acute hemiballismus treated by ventrolateral thalamolysis. Brain 82, 104–108 (1959).
  Article CAS PubMed Google Scholar
• Ehringer, H. & Hornykiewicz, O. Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system. Klin. Wochenschr. 38, 1236–1239 (1960).
  Article CAS PubMed Google Scholar
• Birkmayer, W. & Hornykiewicz, O. The L-3,4-dioxyphenylalanine (DOPA)-effect in Parkinson-akinesia. Wien Klin. Wochenschr. 73, 787–788 (1961).
  CAS PubMed Google Scholar
• Cotzias, G. C., Papavasiliou, P. S. & Gellene, R. L-dopa in Parkinson's syndrome. N. Engl. J. Med. 281, 272 (1969).
  CAS PubMed Google Scholar
• Fahn, S. The history of dopamine and levodopa in the treatment of Parkinson's disease. Mov. Disord. 23, S497–S508 (2008).
  Article PubMed Google Scholar
• Denny-Brown, D. & Yanagisawa, N. in The Basal Ganglia (ed. Yahr, M. D.) 145 (Raven Press, New York, 1976).
  Google Scholar
• Hassler, R. Striatal control of locomotion, intentional actions and of integrating and perceptive activity. J. Neurol. Sci. 36, 187–224 (1978).
  Article CAS PubMed Google Scholar
• Haber, S. N. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26, 317–330 (2003).
  Article PubMed Google Scholar
• Alexander, G. E. in Handbook of Brain Theory and Neural Networks (ed. Arbib, M. A.) 139–144 (MIT Press, Cambridge, Massachusetts, 1995).
  Google Scholar