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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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Neural evidence for automatic value-modulated approach behaviour
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“, 2016c) of value-driven attentional priority as well as the control of motor behaviour (Bromberg-Martin et al., 2010; Dirnberger and Jahanshahi, 2013; Redgrave et al., 2010; Strafella et al., 2003).”
BackgroundHerold, F., Aye, N., Hamacher, D., & Schega, L. (2019) · Brain Topography · doi:10.1007/s10548-019-00699-8 · Cited by 19
Mariani, L., Longueville, S., Girault, J., Hervé, D., & Gervasi, N. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104506 · Cited by 17
“The striatum is the main input structure of the basal ganglia, which play a major role in motor control, and habitual and goal-directed actions (Redgrave et al., 2010).”
BackgroundBaldassarre, G., Caligiore, D., & Mannella, F. (2013) · Springer eBooks · doi:10.1007/978-3-642-39875-9_11 · Cited by 18
“…organisation based on multiple cortical-striatal macro-loops (Figure 2; the striatum is the input stage of basal ganglia) encompassing (Redgrave et al., 2010; Yin and Knowlton, 2006): the limbic loop (involving the ventral striatum, also called accumbens), the associative loop…”
Distinct dopaminergic abnormalities in traumatic brain injury and Parkinson’s disease
Jenkins, P. O., Roussakis, A., Simoni, S. D., Bourke, N., Fleminger, J., Cole, J. H., Piccini, P. P., & Sharp, D. J. (2020) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2019-321759 · Cited by 17
Wu, Y. H., Veerareddy, A., Lee, M. R., Bellucci, G., Camilleri, J. A., Eickhoff, S. B., & Krüeger, F. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.053 · Cited by 17
Spee, B. T. M., Sladky, R., Fingerhut, J., Laciny, A., Kraus, C., Carls‐Diamante, S., Brücke, C., Pelowski, M. J., & Treven, M. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.930293 · Cited by 18
“parallel basal ganglia loops are connected in similar fashion to all cortical areas (Redgrave et al., 2010), the computations they perform should be largely analogous, along the lines of a generic selection and reinforcement process (Redgrave et al.”
BackgroundInfluentialKo, N.-H., Laine, C. M., Fisher, B. E., & Valero‐Cuevas, F. J. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00151 · Cited by 17
A probabilistic, distributed, recursive mechanism for decision-making in the brain
Caballero, J. A., Humphries, M. D., & GURNEY, K. N. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006033 · Cited by 16
“Of note, we have omitted in our mapping the projections from thalamus to striatum [76] or to subthalamic nucleus [77], as well as the intrinsic connections from subthalamic nucleus or from globus pallidus pars externa (globus pallidus in non-primates) to striatum (e.”
BackgroundLi, Y., Pan, X., He, Y., Ruan, Y., Huang, L., Zhou, Y., Hou, Z., He, C., Wang, Z., Zhang, X., et al. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00393 · Cited by 17
“Dysregulation of goal-directed versus habitual behaviors is considered to be a potential mechanism underlying the relapse of drug addiction (Ostlund and Balleine, 2008), obsessive compulsive disorder (Gillan et al., 2011; Robbins et al., 2012; Burguiere et al., 2015), and may contribute to the executive dysfunction in…”
BackgroundDistinct Dynamics of Striatal and Prefrontal Neural Activity During Temporal Discrimination
Kim, J., Kim, D., & Jung, M. W. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00034 · Cited by 17
cAMP-Fyn signaling in the dorsomedial striatum direct pathway drives excessive alcohol use
Ehinger, Y., Morisot, N., Phamluong, K., Sakhai, S. A., Soneja, D., Adrover, M. F., Alvarez, V. A., & Dorit Ron, A. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0712-1 · Cited by 17
“INTRODUCTION The dorsomedial striatum (DMS) is critically involved in processes such as locomotion [1], and goal-directed behaviors [2, 3].”
BackgroundPsychological and Neuroscientific Connections with Reinforcement Learning
Shah, A. (2012) · Adaptation, learning, and optimization · doi:10.1007/978-3-642-27645-3_16 · Cited by 17
Speech Motor Sequence Learning: Acquisition and Retention in Parkinson Disease and Normal Aging
Whitfield, J. A., & Goberman, A. M. (2017) · Journal of Speech Language and Hearing Research · doi:10.1044/2016_jslhr-s-16-0104 · Cited by 16
Sako, W., Abe, T., Furukawa, T., Oki, R., Haji, S., Murakami, N., Izumi, Y., Harada, M., & Kaji, R. (2019) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2019.03.022 · Cited by 17
Zhang, Y., Xu, S., Xiao, G., Song, Y., Gao, F., Wang, M., Zhao, H., Xing, G., & Cai, X. (2019) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2019.127126 · Cited by 17
Divergent encoding of active avoidance behavior in corticostriatal and corticolimbic projections
Kajs, B. L., Loewke, A. C., Dorsch, J. M., Vinson, L. T., & Gunaydin, L. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-14930-3 · Cited by 17
“The striatum consists of D1 and D2 medium spiny neurons (MSNs) that, when optogenetically stimulated, drive motor initiation and motor cessation, respectively (Kravitz & Kreitzer, 2012; Redgrave et al., 2010).”
BackgroundInfluentialHu, B., & Chomiak, T. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.08.004 · Cited by 18
Gonzalo-Martín, E., Alonso-Martínez, C., Prensa, L., & Clascá, F. (2024) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2023.1305500 · Cited by 16
Decomposition of abnormal free locomotor behavior in a rat model of Parkinson's disease
Grieb, B., von Nicolai, C., Engler, G., Sharott, A., Papageorgiou, I. E., Hamel, W., Engel, A. K., & Moll, C. K. E. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00095 · Cited by 16
Brockmeyer, T., Walther, S., Ingenerf, K., Wild, B., Hartmann, M., Weisbrod, M., Weber, M. D., Eckhardt‐Henn, A., Herzog, W., & Friederich, H. (2016) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2016.02.007 · Cited by 16
“Fronto-striatal loops, including the prefrontal and sensorimotor cortex and the striatum subserve cognitive control functions including task switching and response inhibition (Koechlin et al., 2003; Redgrave et al., 2010).”
BackgroundAchiro, J. M., Shen, J., & Bottjer, S. W. (2017) · eLife · doi:10.7554/elife.26973 · Cited by 18
“, 1999; Paterson and Bottjer, 2017) and appear functionally similar to sensorimotor and associative cortico-basal ganglia loops that contribute to different aspects of motor learning in mammals (Thorn et al., 2010; Yin et al., 2008; Samejima and Doya, 2007; Ashby et al., 2010; Redgrave et al., 2010; Graybiel, 2008; Gr…”
InfluentialReduced habit-driven errors in Parkinson’s Disease
Bannard, C., Leriche, M., Bandmann, O., Brown, C. H., Ferracane, E., Sánchez‐Ferro, Á., Obeso, J. A., Redgrave, P., & Stafford, T. (2019) · Scientific Reports · doi:10.1038/s41598-019-39294-z · Cited by 16
Arroyave, J. A. C., Tobón, C., Revelo, J. J. S., Ochoa-Gómez, J. F., Bocanegra, Y., Gómez, L. M., & Salazar, D. A. P. (2019) · Future Neurology · doi:10.2217/fnl-2018-0048 · Cited by 18
Vázquez-Vázquez, H. A., Gónzalez‐Sandoval, C., Vega, A. V., Arias‐Montaño, J., & Barral, J. A. (2020) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-020-00980-6 · Cited by 16
Maidan, I., Mirelman, A., Hausdorff, J. M., Stern, Y., & Habeck, C. G. (2021) · Scientific Reports · doi:10.1038/s41598-021-85058-z · Cited by 16
Impaired Temporal Processing of Tactile and Proprioceptive Stimuli in Cerebellar Degeneration
Tinazzi, M., Morgante, F., Peretti, A., Mariotti, C., Panzeri, M., Fiorio, M., & Fasano, A. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078628 · Cited by 17
“Basal ganglia function is to select between competing options in order to produce either goal-directed or habitual behaviours, which in turn depend on segregated functional territories [32].”
BackgroundA subcortical network for implicit visuo-spatial attention: Implications for Parkinson's Disease
Esposito, M., Tamietto, M., Geminiani, G. C., & Celeghin, A. (2021) · Cortex · doi:10.1016/j.cortex.2021.05.003 · Cited by 16
Scholl, C., Baladron, J., Vitay, J., & Hamker, F. H. (2022) · Brain Structure and Function · doi:10.1007/s00429-021-02446-x · Cited by 16
Cortical oscillatory dysfunction in Parkinson disease during movement activation and inhibition
Disbrow, E. A., Glassy, N., Dressler, E. M., Russo, K., Franz, E. A., Turner, R. S., Ventura, M. I., Hinkley, L. B. N., Zweig, R. M., Nagarajan, S. S., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0257711 · Cited by 15
“For example, abnormalities in motor cortical activity observed in PD [27, 28] have been linked to loss of dopamine in the posterior putamen [29, 30].”
BackgroundContreras-López, R., Alatriste-León, H., Díaz-Hernández, E., Ramírez‐Jarquín, J. O., & Tecuapetla, F. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112000 · Cited by 19
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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