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

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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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Selection of cortical dynamics for motor behaviour by the basal ganglia
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“Among the other structures found activated in SRTT, it has been suggested that the BG are involved in the chunking process as demonstrated in both animals (Levesque et al., 2007; Jog, Kubota, Connolly, Hillegaart, & Graybiel, 1999; Aldridge & Berridge, 1998; Graybiel, 1998; Cromwell & Berridge, 1996; Berridge & Whisha…”
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“In addition, basal ganglia dysfunction is accompanied with motor learning deficits thought to be due, in part, to the inability to construct or express chunked responses (Graybiel, 1995, 1998).”
Background
Recurrent perseveration correlates with abnormal repetitive locomotion in adult mink but is not reduced by environmental enrichment
Dallaire, J. A., Meagher, R. K., Díez‐León, M., Garner, J. P., & Mason, G. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.061 · Cited by 45
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“More specifically, these authors hypothesized that repeated acts of mindfulness, regularly practiced, could lay down circuitry in the habit-forming part of the brain in the basal ganglia (Graybiel, 1998).”
Background
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“This pattern of activation suggests an involvement of basal ganglia circuitry in rule formation, rather than rehearsingwell learned rules or forming long-term memories (Boettiger and D'Esposito, 2005; Graybiel, 1998; Toni and Passingham, 1999; Toni et al., 2001b).”
Background
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“Theme: Neural basis of behavior Topic: Cognition Keywords: Dorsolateral prefrontal cortex Globus pallidus Planning Selective updating”
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Anticipatory reward signals in ventral striatal neurons of behaving rats
Khamassi, M., Mulder, A. B., Tabuchi, E., Douchamps, V., & Wiener, S. I. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06480.x · Cited by 50
“The present results bear on recent theories and models of mechanisms of goal-directed learning engaging basal ganglia activity (Schultz et al., 1997; Graybiel, 1998).”
BackgroundResultInfluential
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“The basal ganglia play a critical role in selecting movements (Graybiel 1998; Gurney et al 2001a, 2001b; Houk 2010; Tunik et al. 2009) and in the scaling of movement amplitudes (Desmurget et al. 2004; Krakauer et al. 2004; see Jueptner and Weiller 1998).”
Influential
Distinct roles of presynaptic dopamine receptors in the differential modulation of the intrinsic synapses of medium-spiny neurons in the nucleus accumbens
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“Intrinsic connections may be viewed as the hidden layer in a Hopfield network [76] – so their modulation would be expected to shape information flow through the area and confer greater compu-”
Background
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Segovia, K. N., Correa, M., Lennington, J. B., Conover, J. C., & Salamone, J. D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08036.x · Cited by 40
“In contrast, it has been suggested that plasticity in the dorsal striatum is involved in later stages of instrumental learning (McDonald & White, 1993; Graybiel, 1998; Packard & Knowlton, 2002; Yin et al., 2005; Yin & Knowlton, 2006), and is critical for the process of habit formation.”
Dynamic Sensorimotor Planning during Long-Term Sequence Learning: The Role of Variability, Response Chunking and Planning Errors
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“Neural models of sequence learning suggest that learning happens by binding independent responses together in a unified action plan [15,45].”
BackgroundResult
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“The cerebellum functions in error correction and control of ongoing movement, whilst the striatum is important for reinforcement learning and motor “chunking” (the process by which sequences of motor actions are concatenated with training [29]).”
Background
Complete representation of action space and value in all dorsal striatal pathways
Weglage, M., Wärnberg, E., Lazaridis, I., Calvigioni, D., Tzortzi, O., & Meletis, K. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109437 · Cited by 44
Negative priming in patients with Parkinson's disease: Evidence for a role of the striatum in inhibitory attentional processes.
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“Neural circuitry in the basal ganglia (BG) is intimately involved in the control of learned behaviors (Graybiel et al., 1994; Graybiel, 1998), and is thought to be essential for the modification of behavior through reinforcement (Barto, 1995; Doya, 2000; Daw and Doya, 2006).”
Background
Advance cueing produces enhanced action-boundary patterns of spike activity in the sensorimotor striatum
Barnes, T. D., Mao, J.-B., Hu, D., Kubota, Y., Dreyer, A. A., Stamoulis, C., Brown, E. N., & Graybiel, A. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00871.2010 · Cited by 40
Dopaminergic Vulnerability in Parkinson Disease: The Cost of Humans’ Habitual Performance
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Rewards and punishments, goal-directed behavior and consciousness
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Parallel and serial processing in dual-tasking differentially involves mechanisms in the striatum and the lateral prefrontal cortex
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Subthalamic and Striatal Neurons Concurrently Process Motor, Limbic, and Associative Information in Rats Performing an Operant Task
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“One interesting hypothesis concerning the role of the basal ganglia in behavior is that they mediate the acquisition of habits or sequences of behavior by coding for the start and stop times of the " chunks " constituting those sequences (Graybiel 1995, 1998, Jog et al. 1999).”
Procedural Learning in Humans ☆
Knowlton, B. J., Siegel, A. L. M., & Moody, T. D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21085-7 · Cited by 45
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“play a key role in this process in vertebrates [1–5].”
Background
Distribution and morphological characteristics of striatal interneurons expressing calretinin in mice: A comparison with human and nonhuman primates
Petryszyn, S., Beaulieu, J., Parent, A., & Parent, M. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.06.002 · Cited by 38
“The striatum is the major integrative component of the basal ganglia, a set of subcortical structures that plays a crucial role in the control of motor activities and rewarded behaviors (Graybiel,1998; Parent and Hazrati, 1995; Schultz, 2002).”
Background

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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