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Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease
Open accessAbstract
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.
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“Conversely, in PD, the early and preferential loss of DA in the dorsal basal ganglia leads to diminished automatic and increased cognitive (frontal cortex) control of motor movements.”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [2]
In the citing paper
“Consequently, individuals with PD must handle and sustain a larger cognitive load to execute either motor or cognitive tasks2, 3.”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [2]
In the citing paper
“In healthy individuals, motor performance is dependent on the interaction between unconscious (automatic) and volitional (cognitive) control of movement 1, 2.”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [2]
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“The basal ganglia and its cortical connections also play an essential role in procedural motor learning, including the acquisition and retention of automaticity (For review see 2, 127).”
From Exercise-enhanced neuroplasticity targeting motor and cognitive circuitry in Parkinson's disease (2013) · cites this paper as [2]
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BackgroundFunctional and spatial rewiring principles jointly regulate context-sensitive computation
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BackgroundHigh-dimensional encoding of movement by single neurons in basal ganglia output
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Parcellation of functional sub-regions from fMRI: A graph clustering based approach
Haq, N. F., Tan, S. N., McKeown, M. J., & Wang, Z. J. (2018) · Biomedical Signal Processing and Control · doi:10.1016/j.bspc.2018.11.007 · Cited by 3
Religion and Frontotemporal Dementia
Block, N., & Miller, B. L. (2019) · Cambridge University Press eBooks · doi:10.1017/9781316014165.016 · Cited by 3
Wree, A., & Schmitt, O. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-397025-1.00215-3 · Cited by 3
Taniuchi, R., Harada, T., Nagatani, H., Makino, T., Watanabe, C., & Kanai, S. (2022) · Clinical Parkinsonism & Related Disorders · doi:10.1016/j.prdoa.2022.100151 · Cited by 3
“Crucially, patients with PD have great difficulty developing habitual control despite repeated practice [23], which strongly suggests that an increase in motor activity without goal-directed control is insufficient to enhance neuroplasticity [29].”
BackgroundThe Role of Feedback in Decision Making
Osman, M. (2011) · InTech eBooks · doi:10.5772/16669 · Cited by 3
“…bear more specifically to PD performance in the decision making tasks, some have claimed that failure to exhibit incremental cue-outcome learning (as in the WPT, or in some cases the IGT) is the result of slower rates of learning (McKinlay et al, 2010; Redgrave et al, 2010; Rutledge et al, 2009).”
BackgroundFinding minimal action sequences with a simple evaluation of actions
Shah, A., & GURNEY, K. N. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2014.00151 · Cited by 3
“…of observed behavior in biological systems may be distributed across different learning and control processes (Dickinson, 1985; Milner et al., 1998; Packard and Knowlton, 2002; Pasupathy and Miller, 2005; Yin et al., 2008; Balleine et al., 2009; Balleine and O’Dohrety, 2010; Redgrave et al., 2010).”
BackgroundBK Channels Reveal Novel Phosphate Sensitivity in SNr Neurons
Ji, J., Chen, L., Duan, X., Song, X., Su, W., Zhang, P., Li, L., Bai, S., Sun, Y., & Inagaki, N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052148 · Cited by 3
“Recently, we showed that BK channels are functional in SNc and LGP (lateral globus pallidus) neurons, and that they are inhibited by IHEPs at negative transmembrane potential, but they are not sensitive to AMP [11,12].”
BackgroundInfluentialElectromyographic analysis of goal-directed grasping behavior in American lobster
Tomina, Y., & Takahata, M. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.107771 · Cited by 3
“Cellular and synaptic mechanisms underlying manipulative behavior have been studied chiefly by operant conditioning of the behavior (e.g. Kelley, 2004; Schultz, 2006; Gazzaniga et al., 2009; Redgrave et al., 2010) with the advantage that the behavior can be reliably repeated by experimenters and its sequence from init…”
BackgroundCortico-Striatal, Cognitive-Motor Interactions Underlying Complex Movement Control Deficits
Kucinski, A. J., & Sarter, M. F. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-3-319-42743-0_6 · Cited by 3
Multi-task prioritization during the performance of a postural–manual and communication task
Simon-Kuhn, K. L., Haddad, J. M., & Huber, J. E. (2019) · Experimental Brain Research · doi:10.1007/s00221-019-05473-7 · Cited by 3
Effect of DBS Targeting Striatum on beta Oscillations in Parkinson’s Disease
Lu, C., Deng, B., Zhu, Y., Wang, J., & Liu, C. (2019) · Chinese Control Conference (CCC) · doi:10.23919/chicc.2019.8866389 · Cited by 3
“GPe not only forms an excitatory-inhibitory loop with the STN, but also interconnects with the striatum [17-24].”
BackgroundEastern Spirituality, Mind–Body Practices and Neuro-Rehabilitation
Yeates, G. (2019) · Cambridge University Press eBooks · doi:10.1017/9781316014165.018 · Cited by 3
Tang, J., Yang, C., Shi, M., & Chen, W. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113759 · Cited by 3
Advances in Therapeutic Options for Gait and Balance in Parkinson’s Disease
Bohnen, N. I., Albin, R. L., Müller, M. L. T. M., & Chou, K. L. (2012) · European Neurological Review · doi:10.17925/enr.2012.07.03.160 · Cited by 3
Scholl, C., Baladron, J., Vitay, J., & Hamker, F. H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.08.430235 · Cited by 3
“The dichotomy between goal-directed and habitual behavior has often been associated with separate cortico-basal ganglia loops through the dorsomedial and dorsolateral striatum (Yin and Knowlton, 2006; Redgrave et al., 2010).”
BackgroundCui, L., Tang, S., Zhao, K., Pan, J., Zhang, Z., Si, B., & Xu, N.-L. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.16.468594 · Cited by 3
Longo, F., Aryal, S., Anastasiades, P. G., Maltese, M., Baimel, C., Albanese, F., Tabor, J., Zhu, J. D., Oliveira, M. M., Gastaldo, D., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.08.519509 · Cited by 3
Gilchrist, M., Kozak, R. A., Prenger, M. T. M., Anello, M., Hedger, K. V., MacDonald, P. A., & Corneil, B. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.27.625399 · Cited by 3
Essoh, A., Gangal, H., Huang, Z., Chen, R., Xie, X., Wang, X., Vierkant, V., Garza, M., Ugartemendia, L., Secci, M. E., et al. (2025) · eLife · doi:10.7554/elife.107145.1 · Cited by 3
Reif, A. E., Summers, D., Whitfield, J. A., & Goberman, A. M. (2023) · Journal of Speech Language and Hearing Research · doi:10.1044/2022_jslhr-22-00435 · Cited by 2
The role of the somatosensory cortex in self-paced movement impairment in Parkinson’s disease
Madetko‐Alster, N., Alster, P., Lamoš, M., Šmahovská, L., Boušek, T., Rektor, I., & Bočková, M. (2025) · Clinical Neurophysiology · doi:10.1016/j.clinph.2025.01.001 · Cited by 2
“One theory explaining movement impairment among PD patients suggests a shift toward associative motor control even for executing habitual movements (Redgrave et al., 2010).”
Subthalamic Activity Is Associated With Proactive Inhibition in Parkinson's Disease Patients
Damiani, L., Albares, M., Laviron, P., Douget, J.-E. L., Boulinguez, P., Karachi, C., Welter, M., Munuera, J., & Lau, B. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70055 · Cited by 2
“More severely affected patients tend to lose motor automaticity and rely on more cognitive control of action (Redgrave et al. 2010; Wu et al. 2015).”
Eye movements during the Iowa Gambling Task in Parkinson’s disease: a brief report
Doshier, K., Ryals, A., Nejtek, V., Salvatore, M. F., & Lisk, J. P. (2025) · Frontiers in Psychology · doi:10.3389/fpsyg.2025.1478500 · Cited by 1
“A substantial reduction in blink rate may reflect disrupted dopaminergic and norepinephrinergic function, which plays a role in both motor control and cognitive processing (Van Slooten et al., 2019; Jongkees and Colzato, 2016; Willett et al., 2023; Redgrave et al., 2010).”
Essoh, A., Xie, X., Gangal, H., Huang, Z., Chen, R., Li, Z., Wang, X., Vierkant, V., Garza, M., Ugartemendia, L., et al. (2026) · eLife · doi:10.7554/elife.107145.3 · Cited by 2
Wang, Z., Liu, Y., Li, C., Qin, K., Yu, X., & Xie, A. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.06.057 · Cited by 2
Sanchiz-Calvo, M., Coccia, E., Cawthorne, C., Parfitt, G. M., Torre-Muruzabal, T., Tsafaras, G., Laere, K. V., Cabezudo, D., Cascalho, A. C. C., den Haute, C. V., et al. (2025) · Acta Neuropathologica · doi:10.1007/s00401-025-02908-0 · Cited by 2
“This pathway contributes to the basal ganglia circuits involved in action selection, modulation and learning [1, 23].”
Köchli, S., Casso, M.-I., Delevoye, Y., Schmid, S., Rose, D., & Whyatt, C. P. (2025) · Sensors · doi:10.3390/s25195999 · Cited by 2
“Previous neurological evidence suggests that dopaminergic neuron loss in PD disrupts the balance between habitual and goal-directed actions [74,75].”
White matter hyperintensities drive propagating grey matter atrophy in cerebral small vessel disease
Mu, R., Yang, P., Qin, X., Zheng, W., Lv, J., Huang, B., Li, X., Feng, Y., Huang, D., Li, P., et al. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf429 · Cited by 2
Increased basal ganglia volume in older adults with tinnitus
Martín, S. S., Medel, V., Breinbauer, H. A., Delgado, C., & Delano, P. H. (2025) · Scientific Reports · doi:10.1038/s41598-025-25065-6 · Cited by 2
“Importantly, these patients did not complain about tinnitus, as they were recruited from primary care adult health screening programs, representing a specific subset of “sensorial tinnitus” in older adults.”
Impairment in stimulus-response learning as a cognitive biomarker in a model of synucleinopathy
Princz‐Lebel, O., Attaran, A., Contreras, R. S., Novikov, V., Panjwani, S., Chu, A., Tan, C., Lemieux, C. A., Skirzewski, M., Machado, M. M. F., et al. (2026) · Translational Psychiatry · doi:10.1038/s41398-025-03795-5 · Cited by 2
Neuromodulation of Cortical Targets in Freezing of Gait
Revuelta, G. J., Lench, D. H., Silva‐Batista, C., Dale, M. L., & Mancini, M. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70406 · Cited by 2
“Reliance on these cognitive control networks aligns with evidence that people with PD increasingly depend on executive resources and external cues in order to generate effective locomotion by switching to goal-directed behavior (Redgrave et al. 2010; Gilat et al. 2021).”
Kim, M., Youm, C., Park, H., Kim, B., Choi, H., Hwang, J., & Cheon, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-45122-y · Cited by 2
“…are thought to arise from dysfunction within the basal ganglia circuitry resulting from reduced dopaminergic neurotransmission, which leads to impaired movement planning and a diminished capacity to maintain automatic motor patterns during gait, postural transitions, and balance control 26,27 .”
Yoo, H. S., Kim, H., Park, M., Ahn, S. J., Lee, J., Ryu, Y. H., & Lyoo, C. H. (2026) · Neurology · doi:10.1212/wnl.0000000000214812 · Cited by 2
Prediction error correlates in the striosome-dopamine circuit emerge from information gain
Beck, D. W., & Friedman, A. (2026) · Nature Communications · doi:10.1038/s41467-026-73994-1 · Cited by 2
“↓ dopamine:bluntedupdatingandlearningde fi cits(likein PD 193 ). e Early in standard associative learning (top box), policy-IG issues three signals when a novel stimulus (green cheese) appears: encode predictive cues ( “ bell → cheese ” ),integratethestimulusintoactionselection( “ ↑ eat ” ),and…”
Metadata
- Authors
- Redgrave, P., Rodriguez, M., Smith, Y., Rodriguez-Oroz, M. C., Lehericy, S., Bergman, H., Agid, Y., DeLong, M. R., & Obeso, J. A.
- Affiliations
- University of Sheffield (GB)
- Emory University (US)
- Hebrew University of Jerusalem (IL)
- Institut du Cerveau (FR)
- Biomedical Research Networking Center on Neurodegenerative Diseases (ES)
- Corresponding author
- Redgrave, Peter
- Obeso, Jose A.
- Venue
- Nature reviews. Neuroscience
- Published
- 2010-10-14
- Volume
- 11
- Issue
- 11
- Pages
- 760-772
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC3124757
- OpenAlex
- W2056061278
- Cited by
- 1,134
- References
- 178
- Citations by year
- 2026: 59 · 2025: 78 · 2024: 74 · 2023: 70 · 2022: 90 · 2021: 78 · 2020: 75 · 2019: 122 · 2018: 64 · 2017: 62 · 2016: 73 · 2015: 65 · 2014: 72 · 2013: 68 · 2012: 47
- FWCI
- 6.08
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Deposito Adademico Digital Universidad De Navarra (University of Navarra) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (091409)
- Universidad de Navarra
- Topics
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- basal ganglia, Parkinson's disease, goal-directed behavior, habitual behavior, dopamine depletion, posterior putamen, action control
- MeSH terms
- Animals, Basal Ganglia, Goals, Habituation, Psychophysiologic, Humans, Models, Neurological, Nerve Net, Neural Pathways, Parkinson Disease
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