The Basal Ganglia and Chunking of Action Repertoires

Graybiel, Ann M.

doi:10.1006/nlme.1998.3843

Cited by 1,042Memory and Neural MechanismsMotor Control and AdaptationNeural and Behavioral Psychology Studies

The Basal Ganglia and Chunking of Action Repertoires

Graybiel, Ann M.·1998·Neurobiology of Learning and Memory

DOI 10.1006/nlme.1998.3843

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Abstract

The basal ganglia have been shown to contribute to habit and stimulus-response (S-R) learning. These forms of learning have the property of slow acquisition and, in humans, can occur without conscious awareness. This paper proposes that one aspect of basal ganglia-based learning is the recoding of cortically derived information within the striatum. Modular corticostriatal projection patterns, demonstrated experimentally, are viewed as producing recoded templates suitable for the gradual selection of new input-output relations in cortico-basal ganglia loops. Recordings from striatal projection neurons and interneurons show that activity patterns in the striatum are modified gradually during the course of S-R learning. It is proposed that this recoding within the striatum can chunk the representations of motor and cognitive action sequences so that they can be implemented as performance units. This scheme generalizes Miller's notion of information chunking to action control. The formation and the efficient implementation of action chunks are viewed as being based on predictive signals. It is suggested that information chunking provides a mechanism for the acquisition and the expression of action repertoires that, without such information compression would be biologically unwieldy or difficult to implement. The learning and memory functions of the basal ganglia are thus seen as core features of the basal ganglia's influence on motor and cognitive pattern generators.

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The basal ganglia are important for chunking action sequences.
“It has been suggested that the basal ganglia are important for chunking action sequences (Graybiel, 1998).”
From The Neural Correlates of Motor Skill Automaticity (2005) · cites this paper as Graybiel, 1998
Decreased activity in the basal ganglia may reflect a more effective (chunked) representation that accompanies automatization.
“Thus, decreased activity in the basal ganglia may reflect a more effective (chunked) representation that accompanies automatization.”
From The Neural Correlates of Motor Skill Automaticity (2005) · cites this paper as Graybiel, 1998
Stimulus-response or habit learning appears to be mediated, in part, by the dorsolateral striatum (or the putamen).
“This learning process appears to be mediated, in part, by the dorsolateral striatum (or the putamen) (Knowlton et al., 1996; White, 1997; Graybiel, 1998; Hikosaka, 1998; Yin and Knowlton, 2006).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Graybiel, 1998

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NEURAL MECHANISMS OF ADDICTION: The Role of Reward-Related Learning and Memory
Hyman, S. E., Malenka, R. C., & Nestler, E. J. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113009 · Cited by 2,647 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
Self-citation
Learning and Memory Functions of the Basal Ganglia
Packard, M. G., & Knowlton, B. J. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142937 · Cited by 1,717 · see citing works
The mGluR theory of fragile X mental retardation
Bear, M. F., Huber, K. M., & Warren, S. T. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.04.009 · Cited by 1,580 · see citing works
Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Psychology of Habit.
Wood, W., & Rünger, D. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-122414-033417 · Cited by 1,445 · see citing works
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
A new look at habits and the habit-goal interface.
Wood, W., & Neal, D. T. (2007) · Psychological Review · doi:10.1037/0033-295x.114.4.843 · Cited by 1,470 · see citing works
The mysterious motivational functions of mesolimbic dopamine
Salamone, J. D., & Correa, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.021 · Cited by 1,418 · see citing works
Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning
Yin, H. H., Knowlton, B. J., & Balleine, B. W. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03095.x · Cited by 1,226 · see citing works
Addiction, Dopamine, and the Molecular Mechanisms of Memory
Berke, J. D., & Hyman, S. E. (2000) · Neuron · doi:10.1016/s0896-6273(00)81056-9 · Cited by 1,167 · see citing works
The role of the dorsomedial striatum in instrumental conditioning
Yin, H. H., Ostlund, S. B., Knowlton, B. J., & Balleine, B. W. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04218.x · Cited by 1,099 · see citing works
Neural mechanisms of language comprehension: Challenges to syntax
Kuperberg, G. R. (2006) · Brain Research · doi:10.1016/j.brainres.2006.12.063 · Cited by 1,033 · see citing works
Cybernetic Big Five Theory
DeYoung, C. G. (2015) · Journal of Research in Personality · doi:10.1016/j.jrp.2014.07.004 · Cited by 1,057 · see citing works
Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits
Salamone, J. D., Correa, M., Farrar, A., & Mingote, S. M. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0668-9 · Cited by 1,000 · see citing works
Addiction: A Disease of Learning and Memory
Hyman, S. E. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.8.1414 · Cited by 980 · see citing works
Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation
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a neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Promoting habit formation
Lally, P., & Gardner, B. (2013) · Health Psychology Review · doi:10.1080/17437199.2011.603640 · Cited by 901 · see citing works
Central mechanisms of motor skill learning
Hikosaka, O., Nakamura, K., Sakai, K., & Nakahara, H. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00307-0 · Cited by 1,023 · see citing works
Toward a neurobiology of obsessive-compulsive disorder
Graybiel, A. M., & Rauch, S. L. (2000) · Neuron · doi:10.1016/s0896-6273(00)00113-6 · Cited by 864 · see citing works
Self-citation
Building neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834 · see citing works
The Cartography of Syntactic Structures
Cinque, G., & Rizzi, L. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199544004.013.0003 · Cited by 834 · see citing works
The cerebellum communicates with the basal ganglia
Hoshi, E., Tremblay, L., Féger, J., Carras, P. L., & Strick, P. L. (2005) · Nature Neuroscience · doi:10.1038/nn1544 · Cited by 833 · see citing works
Different time courses of learning-related activity in the prefrontal cortex and striatum.
Pasupathy, A., & Miller, E. K. (2005) · Nature · doi:10.1038/nature03287 · Cited by 712 · see citing works
The Now-or-Never bottleneck: A fundamental constraint on language
Christiansen, M. H., & Nick Chater, A. (2015) · Behavioral and Brain Sciences · doi:10.1017/s0140525x1500031x · Cited by 750 · see citing works
Hierarchically organized behavior and its neural foundations: A reinforcement learning perspective
Botvinick, M. M., Niv, Y., & Barto, A. G. (2009) · Cognition · doi:10.1016/j.cognition.2008.08.011 · Cited by 646 · see citing works
Move to the rhythm: oscillations in the subthalamic nucleus–external globus pallidus network
Bevan, M. D. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02235-x · Cited by 633 · see citing works
The Oxford Handbook of Linguistic Analysis
Heine, B., & Narrog, H. (2009) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199544004.001.0001 · Cited by 646 · see citing works
Start/stop signals emerge in nigrostriatal circuits during sequence learning
Jin, X., & Costa, R. M. (2010) · Nature · doi:10.1038/nature09263 · Cited by 611 · see citing works
Behavioral functions of the mesolimbic dopaminergic system: An affective neuroethological perspective
Alcaro, A., Huber, R., & Panksepp, J. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.07.014 · Cited by 614 · see citing works
Why ritualized behavior? Precaution Systems and action parsing in developmental, pathological and cultural rituals
Boyer, P., & Liénard, P. (2006) · Behavioral and Brain Sciences · doi:10.1017/s0140525x06009332 · Cited by 601 · see citing works
Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories
Barnes, T. D., Kubota, Y., Hu, D., Jin, D. Z., & Graybiel, A. M. (2005) · Nature · doi:10.1038/nature04053 · Cited by 595 · see citing works
The Neural Correlates of Motor Skill Automaticity
Poldrack, R. A., Sabb, F. W., Foerde, K., Tom, S. M., Asarnow, R. F., Bookheimer, S. Y., & Knowlton, B. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3880-04.2005 · Cited by 594 · see citing works
The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy
Schmahmann, J. D. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9142-x · Cited by 583 · see citing works
Fiber Pathways of the Brain
Schmahmann, J. D., & Pandya, D. N. (2006) · doi:10.1093/acprof:oso/9780195104233.001.0001 · Cited by 1,157 · see citing works
Increased Synaptic Dopamine Function in Associative Regions of the Striatum in Schizophrenia
Kegeles, L. S., Abi-Dargham, A., Frankle, W. G., Gil, R., Cooper, T. B., Slifstein, M., Hwang, D.-R., Huang, Y., Haber, S. N., & Laruelle, M. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.10 · Cited by 565 · see citing works
Obsessive-compulsive disorder: Puzzles and prospects
Robbins, T. W., Vaghi, M. M., & Banca, P. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.046 · Cited by 510 · see citing works
Clinical handbook of mindfulness
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The Neural Representation of Sequences: From Transition Probabilities to Algebraic Patterns and Linguistic Trees
Dehaene, S., Meyniel, F., Wacongne, C., Wang, L., & Pallier, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.019 · Cited by 478 · see citing works
Space and Time: The Hippocampus as a Sequence Generator
Buzsáki, G., & Tingley, D. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.07.006 · Cited by 461 · see citing works
Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum
Lovinger, D. M. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.01.008 · Cited by 488 · see citing works
Brain development and ADHD
Krain, A. L., & Castellanos, F. X. (2006) · Clinical Psychology Review · doi:10.1016/j.cpr.2006.01.005 · Cited by 495 · see citing works
Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences
Jin, X., Tecuapetla, F., & Costa, R. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3632 · Cited by 499 · see citing works
A Possible Role for the Striatum in the Pathogenesis of the Cognitive Symptoms of Schizophrenia
Simpson, E. H., Kellendonk, C., & Kandel, E. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.014 · Cited by 478 · see citing works
Recent advances in Tourette syndrome research
Albin, R. L., & Mink, J. W. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.01.001 · Cited by 478 · see citing works
Action, Outcome, and Value
Cushman, F. A. (2013) · Personality and Social Psychology Review · doi:10.1177/1088868313495594 · Cited by 472 · see citing works
Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning
YIN, H., KNOWLTON, B., & BALLEINE, B. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.07.012 · Cited by 532 · see citing works
The striatum: where skills and habits meet
Graybiel, A. M., & Grafton, S. T. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021691 · Cited by 463 · see citing works
Neurons in the Thalamic CM-Pf Complex Supply Striatal Neurons With Information About Behaviorally Significant Sensory Events
Matsumoto, N., Minamimoto, T., Graybiel, A. M., & Kimura, M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.2.960 · Cited by 451 · see citing works
A Frames Approach to Semantic Analysis
Fillmore, C. J., & Baker, C. F. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199544004.013.0013 · Cited by 456 · see citing works
The Striatum Organizes 3D Behavior via Moment-to-Moment Action Selection
Markowitz, J. E., Gillis, W. F., Beron, C. C., Neufeld, S. Q., Robertson, K., Bhagat, N. D., Peterson, R. E., Peterson, E., Hyun, M., Linderman, S. W., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.019 · Cited by 422 · see citing works
Evidence for a distributed hierarchy of action representation in the brain
Grafton, S. T., & de C. Hamilton, A. F. (2007) · Human Movement Science · doi:10.1016/j.humov.2007.05.009 · Cited by 503 · see citing works
The importance of habits in eating behaviour. An overview and recommendations for future research
Riet, J. V., Sijtsema, S. J., Dagevos, H., & De Bruijn, G.-J. (2011) · Appetite · doi:10.1016/j.appet.2011.07.010 · Cited by 399 · see citing works
Motor Abilities in Autism: A Review Using a Computational Context
Gowen, E., & Hamilton, A. F. D. C. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1574-0 · Cited by 405 · see citing works
Complementary Contributions of Striatal Projection Pathways to Action Initiation and Execution
Tecuapetla, F., Jin, X., Lima, S. Q., & Costa, R. M. (2016) · Cell · doi:10.1016/j.cell.2016.06.032 · Cited by 396 · see citing works
Basal ganglia orient eyes to reward
Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377 · see citing works
A unified framework for addiction: Vulnerabilities in the decision process
Redish, A. D., Jensen, S., & Johnson, A. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0800472x · Cited by 501 · see citing works
Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning
Penhune, V. B., & Steele, C. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.044 · Cited by 373 · see citing works
The nucleus accumbens as part of a basal ganglia action selection circuit
Nicola, S. M. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0510-4 · Cited by 360 · see citing works
A Rap guanine nucleotide exchange factor enriched highly in the basal ganglia
Kawasaki, H., Springett, G. M., Toki, S., Canales, J. J., Harlan, P. C., Blumenstiel, J. P., Chen, E. J., Bany, I. A., Mochizuki, N., Ashbacher, A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.22.13278 · Cited by 353 · see citing works
Obsessive-compulsive disorder
Stein, D. J. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09620-4 · Cited by 352 · see citing works
A dual operator view of habitual behavior reflecting cortical and striatal dynamics
Smith, K. S., & Graybiel, A. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.038 · Cited by 324 · see citing works
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The Evolution of Human Speech
LIEBERMAN, P. H. (2007) · Current Anthropology · doi:10.1086/509092 · Cited by 347 · see citing works
Motivation, reward, and Parkinson's disease: influence of dopatherapy
Czernecki, V. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00108-2 · Cited by 338 · see citing works
Proprioception and Motor Control in Parkinson's Disease
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Brain imaging of attention deficit/hyperactivity disorder
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Sleep-dependent learning and motor-skill complexity
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Dissociating the role of the medial and lateral anterior prefrontal cortex in human planning
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A key role of the basal ganglia in pain and analgesia - insights gained through human functional imaging
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Frontal cortex and the discovery of abstract action rules
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Dissecting the Brain's Internal Clock: How Frontal–Striatal Circuitry Keeps Time and Shifts Attention
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On the nature and evolution of the neural bases of human language
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Motor learning in Parkinson's disease: limitations and potential for rehabilitation
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Sequential super-stereotypy of an instinctive fixed action pattern in hyper-dopaminergic mutant mice: a model of obsessive compulsive disorder and Tourette’s
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Chunking during human visuomotor sequence learning
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Swinging in the brain: shared neural substrates for behaviors related to sequencing and music
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Striatal Circuits as a Common Node for Autism Pathophysiology
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Habits, action sequences and reinforcement learning
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Non-motor basal ganglia functions: A review and proposal for a model of sensory predictability in auditory language perception
Kotz, S. A., Schwartze, M., & Schmidt‐Kassow, M. (2009) · Cortex · doi:10.1016/j.cortex.2009.02.010 · Cited by 297 · see citing works
GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons
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Selective Activation of Striatal Fast-Spiking Interneurons during Choice Execution
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Evolutionary Conservation of the Basal Ganglia as a Common Vertebrate Mechanism for Action Selection
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Molecular imaging of the dopaminergic system and its association with human cognitive function.
Cropley, V., Fujita, M., Innis, R., & Nathan, P. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.004 · Cited by 299 · see citing works
Turning off cortical ensembles stops striatal Up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo
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The persistence of maladaptive memory: Addiction, drug memories and anti-relapse treatments
Milton, A. L., & Everitt, B. J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.01.002 · Cited by 279 · see citing works
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How do the basal ganglia contribute to categorization? Their roles in generalization, response selection, and learning via feedback
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How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades
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Applying Intelligence to the Reflexes: Embodied Skills and Habits between Dreyfus and Descartes
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Motor Memory Consolidation in Sleep Shapes More Effective Neuronal Representations
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Integrating hippocampus and striatum in decision-making
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Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task
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ARTICLE NO. NL983843 The Basal Ganglia and Chunking of Action Repertoires
Grabiel, A. M. (2008)
Building action repertoires: memory and learning functions of the basal ganglia
Graybiel, A. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80100-6 · Cited by 557 · see citing works
Role of the basal ganglia in innate and learned behavioural sequences
Favila, N., GURNEY, K. N., & Overton, P. G. (2023) · Reviews in the Neurosciences · doi:10.1515/revneuro-2023-0038 · Cited by 13 · see citing works
The striatum: where skills and habits meet
Graybiel, A. M., & Grafton, S. T. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021691 · Cited by 463 · see citing works
Shaping action sequences in basal ganglia circuits
Jin, X., & Costa, R. M. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.06.011 · Cited by 194 · see citing works

Authors: Graybiel, A. M.
Affiliations: Massachusetts Institute of Technology (US)
Corresponding author: Graybiel, Ann M.
ORCID: Graybiel, Ann M.
Venue: Neurobiology of Learning and Memory
Publisher: Elsevier BV
Published: 1998-07
Volume: 70
Issue: 1-2
Pages: 119-136
ISSN: 1074-7427 (ISSN-L)
DOI: 10.1006/nlme.1998.3843
OpenAlex: W2148201341
Cited by: 1,042
References: 103
Citations by year: 2026: 25 · 2025: 32 · 2024: 31 · 2023: 48 · 2022: 26 · 2021: 47 · 2020: 36 · 2019: 25 · 2018: 37 · 2017: 39 · 2016: 42 · 2015: 43 · 2014: 41 · 2013: 37 · 2012: 84
FWCI: 8.82
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Neurobiology of Learning and Memory (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (R03 MH57878, R01 NS25529)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: basal ganglia, striatum, repertoires of action, habit learning, stimulus-response learning, corticostriatal projections, striatal projection neurons, striatal interneurons, predictive signals
MeSH terms: Animals, Basal Ganglia, Brain Mapping, Corpus Striatum, Habits, Humans, Learning, Memory, Models, Neurological, Nerve Net, Synaptic Transmission, Neuronal Plasticity, Obsessive-Compulsive Disorder, Parkinson Disease, Neocortex, In Vitro Techniques

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The Basal Ganglia and Chunking of Action Repertoires

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