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Cited by 481Memory and Neural MechanismsMotor Control and AdaptationNeural and Behavioral Psychology Studies

Cortical and basal ganglia contributions to habit learning and automaticity

Open access
Ashby, F. Gregory, Turner, Benjamin O., Horvitz, Jon C.·2010·Trends in Cognitive Sciences
DOI 10.1016/j.tics.2010.02.001PMC PMC2862890
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Abstract

The 20th century was dominated by the view that novel behaviors are mediated primarily in cortex and that the development of automaticity is a process of transferring control to subcortical structures. Much evidence suggests however, that subcortical structures, such as the striatum, make significant contributions to initial learning. More recently, evidence has been accumulating that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensorimotor striatum are more active after automaticity has developed. At the same time, other recent reports suggest that automatic behaviors are striatum- and dopamine-independent, and may be mediated entirely within cortex. Resolving this apparent conflict should be a major goal of future research.

AI snapshot

Written from the paper’s full text.

TL;DR

The review argues that the classical view—novel behaviors are cortical and automaticity is a transfer to subcortical control—is too simple. It highlights evidence that associative striatum contributes early in learning, sensorimotor striatum is more active after over-learning in some tasks, yet other findings suggest automatic behaviors can become striatum- and dopamine-independent and may be mediated by cortical-cortical networks.

Key findings

  • The associative striatum is especially active early in skill learning: Miyachi, Hikosaka, and Lu found most striatal neurons responding more strongly during early learning were in associative striatum; temporary inactivation disrupted learning of new motor sequences but had less effect on previously acquired sequences, and lesions produced premature S-R-like habit performance with bar-pressing unaffected by outcome devaluation.
  • The sensorimotor striatum shows the opposite pattern in some studies: most neurons responding more strongly after over-learning were in sensorimotor striatum; inactivation disrupted execution of previously acquired sequences but not new learning, and lesions prevented the shift from goal-directed action to S-R habit. However, task type matters: sequence-learning fMRI studies reported increased sensorimotor striatal activation with extended training, whereas single-response tasks reported decreased task-related neurons, with Carelli et al. showing cells ceased responding after automaticity was established.
  • Dopamine supports cortico-striatal reinforcement learning: phasic dopamine increases follow unexpected rewards and depress below baseline after unexpected reward omission; D1 receptor blockade strongly disrupts early Pavlovian approach but has little effect after extended training. In prefrontal cortex, dopamine clearance is slow—one food pellet elevated dopamine for approximately 30 minutes—which the authors say rules out dopamine as a trial-by-trial reinforcement signal in cortex.
  • Cortical practice effects are mixed: decreases often occur in prefrontal and parietal attentional-control areas, increases in premotor and motor areas during motor tasks, and redistributions occur when cognitive processes differ early versus late. Inactivation of infralimbic cortex makes well-acquired S-R habits become goal-directed, and one model proposes basal ganglia train cortical-cortical representations so control gradually passes to a faster cortical path.

Methods

  • Narrative review/synthesis, not an empirical study; it focuses on cortical and basal ganglia contributions to habit learning and automaticity in simple motor and cognitive tasks.
  • Evidence discussed includes animal single-unit recording, lesion and temporary inactivation studies, fMRI/PET human neuroimaging, pharmacological dopamine manipulations, and computational/neurobiological models.
  • Main analysis is qualitative integration of cited findings; no formal meta-analysis or new data are reported.

Limitations

  • The paper states that automaticity is challenging to study, experiments are expensive in time and resources, and the phenomenon involves changes across widely distributed neural networks rather than a single brain region.
  • The paper states that the most pressing open question is resolving the apparent conflict between results showing an enduring role for sensorimotor striatum and results suggesting automatic behaviors become striatum- and dopamine-independent; it also notes that criteria for “automatic” versus “habit” have not been systematically compared and may not identify the same behaviors.
  • Evident from the text: this is a selective narrative review that explicitly excludes complex cognitive, social, and athletic domains and cerebellar contributions, and it does not provide a quantitative synthesis across studies.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.tics.2010.02.001

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 109 cited sources checked · 0 supported · 0 flagged

  • Findingnone given

    Neurons in the associative striatum are selectively activated during early learning.

    “More recently, evidence has been accumulating that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensorimotor striatum are more active after automaticity has developed.”
    Quote in the paperSubstantial claim
  • Findingcitation

    Activation in the associative striatum decreases with extended training.

    “Several fMRI experiments subsequently reported a similar finding – that is, that activation in the associative striatum decreases with training [15–17].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [15] Lehéricy, 2005, Distinct basal ganglia territories are engaged in early and advanced motor sequence learning, Proc. Natl. Acad. Sci. U. S. A. source

      Not checked in the free run.

    • cites [16] Poldrack, 2005, The neural correlates of motor skill automaticity, J. Neurosci. source

      Not checked in the free run.

    • cites [17] Wu, 2004, How self-initiated memorized movements become automatic: A functional MRI study, J. Neurophysiol. source

      Not checked in the free run.

  • Findingnone given

    Neurons in the sensorimotor striatum are more active after automaticity has developed.

    “More recently, evidence has been accumulating that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensorimotor striatum are more active after automaticity has developed.”
    Quote in the paperSubstantial claim
  • Findingcitation

    The associative striatum is active during initial skill acquisition.

    “Several studies have reported that the associative striatum is active during initial skill acquisition and that its activity decreases with extended training.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [14] Miyachi, 2002, Differential activation of monkey striatal neurons in the early and late stages of procedural learning, Exp. Brain Res. source

      Not checked in the free run.

    • cites [15] Lehéricy, 2005, Distinct basal ganglia territories are engaged in early and advanced motor sequence learning, Proc. Natl. Acad. Sci. U. S. A. source

      Not checked in the free run.

    • cites [16] Poldrack, 2005, The neural correlates of motor skill automaticity, J. Neurosci. source

      Not checked in the free run.

    • cites [17] Wu, 2004, How self-initiated memorized movements become automatic: A functional MRI study, J. Neurophysiol. source

      Not checked in the free run.

  • Findingcitation

    Most striatal neurons that responded more strongly during early learning were in the associative striatum.

    “Most of the striatal neurons that responded more strongly during early learning were in the associative striatum (Figure 1).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [14] Miyachi, 2002, Differential activation of monkey striatal neurons in the early and late stages of procedural learning, Exp. Brain Res. source

      Not checked in the free run.

  • May combine two claims. 15
  • Classified as probably not a substantial claim. 7

  • May combine two claims.

    Findingcitation

    Temporary inactivation of the associative striatum disrupts learning of new motor sequences but has less effect on execution of previously-acquired sequences.

    “Evidence supporting a role for the associative striatum in behavioral acquisition was reported by Miyachi et al. [18], who found that temporary inactivation of the associative striatum disrupted learning of new motor sequences, but had less effect on the execution of previously-acquired sequences.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Miyachi, 1997, Differential roles of monkey striatum in learning of sequential hand movement, Exp. Brain Res. source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Temporary inactivation of the sensorimotor striatum does not interfere with learning of new motor sequences but disrupts execution of previously-acquired sequences.

    “Furthermore, temporary inactivation of the sensorimotor striatum does not interfere with the learning of new motor sequences, but it does disrupt the execution of previously-acquired sequences [18].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Miyachi, 1997, Differential roles of monkey striatum in learning of sequential hand movement, Exp. Brain Res. source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Dopamine cells exhibit phasic increases in discharge rate following unexpected primary or conditioned rewards and depress their discharge below baseline following an unexpected failure to receive a reward.

    “An extensive literature shows that dopamine cells exhibit phasic increases in discharge rate following unexpected primary or conditioned rewards and depress their discharge below baseline following an unexpected failure to receive a reward [34, 36].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [34] Doya, 2007, Reinforcement learning: Computational theory and biological mechanisms, HFSP J. source

      Not checked in the free run.

    • cites [36] Schultz, 2002, Getting formal with dopamine and reward, Neuron source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Disconnecting the bird homologue of the basal ganglia completely blocks new song learning but has little effect on the expression of well-learned songs.

    “Several studies have shown that disconnecting the bird homologue of the basal ganglia completely blocks new song learning, but has little effect on the expression of well-learned songs (see [31] for a review).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [31] Doupe, 2005, Birdbrains could teach basal ganglia research a new song, Trends Neurosci. source

      Not checked in the free run.

    • Rests on an assumption: The bird homologue of the basal ganglia is functionally comparable to the mammalian basal ganglia for song learning and expression.

  • May combine two claims.

    Findingcitation

    The number of striatal cells showing task-related activations decreases dramatically over the course of operant stimulus-response learning, as focused activity time-locked to task-related events emerges in a select group of striatal cells.

    “As noted above, the number of striatal cells showing task-related activations decreases dramatically over the course of operant S-R learning, as focused activity time-locked to task-related events emerges in a select group of striatal cells [23–24].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [23] Barnes, 2005, Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories, Nature source

      Not checked in the free run.

    • cites [24] Tang, 2007, Changes in activity of the striatum during formation of a motor habit, Eur. J. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Depending on the task, neuroimaging studies have reported a general decrease in cortical activity, increases in cortical activity, or a more complex redistribution where activity increases in some areas and decreases in others during practice.

    “Depending on the task, some studies have reported a general decrease in cortical activity [52–55], a few have reported increases [56–59], and some have reported a more complex redistribution where activity increases in some areas and decreases in others [60–62].”
    Quote in the paperSubstantial claim0 of 10 sources checked
    • cites [52] Jansma, 2001, Functional anatomical correlates of controlled and automatic processing, J. Cogn. Neurosci. source

      Not checked in the free run.

    • cites [53] Hempel, 2004, Plasticity of cortical activation related to working memory during training, Am. J. Psychiatry. source

      Not checked in the free run.

    • cites [54] Toni, 2001, Learning arbitrary visuomotor associations: temporal dynamic of brain activity, Neuroimage source

      Not checked in the free run.

    • cites [55] Toni, 2002, Changes of corticostriatal effective connectivity during visuomotor learning, Cereb. Cortex source

      Not checked in the free run.

    • cites [56] Karni, 1995, Functional MRI evidence for adult motor cortex plasticity during motor skill learning, Nature source

      Not checked in the free run.

    • cites [57] Hazeltine, 1997, Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study, Brain source

      Not checked in the free run.

    • cites [58] Honda, 1998, Dynamic cortical involvement in implicit and explicit motor sequence learning. A PET study, Brain source

      Not checked in the free run.

    • cites [59] Iacoboni, 1996, Brain–behavior relationships: evidence from practice effects in spatial stimulus-response compatibility, J. Neurophysiol. source

      Not checked in the free run.

    • cites [60] Poldrack, 1998, The neural basis of visual skill learning: an fMRI study of mirror reading, Cereb. Cortex source

      Not checked in the free run.

    • cites [61] Poldrack, 2001, Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading, Brain source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation

    Blockade of D1 receptors strongly disrupts rats' performance of a simple Pavlovian approach response to a sensory cue during early stages of training but has little or no disruptive effect in rats that receive extended training prior to dopamine antagonist challenge.

    “As another example, blockade of D1 receptors strongly disrupts rats' performance of a simple Pavlovian approach response to a sensory cue during early stages of training, but has little or no disruptive effect in rats that receive extended training prior to dopamine antagonist challenge [46–47].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [46] Choi, 2005, Extended habit training reduces dopamine mediation of appetitive response expression, J. Neurosci. source

      Not checked in the free run.

    • cites [47] Bespalov, 2007, AMPA receptor antagonists reverse effects of extended habit training on signaled food approach responding in rats, Psychopharmacology (Berl) source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingcitation

    Kelly and Garavan noted that decreases are often observed in prefrontal and parietal areas associated with attentional control, increases have generally been seen in premotor and motor areas during motor tasks, and a redistribution is often found in tasks where different cognitive processes operate during early and late training.

    “Kelly and Garavan [51] noted that decreases are often observed in prefrontal and parietal areas associated with attentional control, increases have generally been seen in premotor and motor areas during motor tasks, and a redistribution is often found in tasks where different cognitive processes operate during early and late training [61, 63].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [51] Kelly, 2005, Human functional neuroimaging of brain changes associated with practice, Cereb. Cortex source

      Not checked in the free run.

    • cites [61] Poldrack, 2001, Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading, Brain source

      Not checked in the free run.

    • cites [63] Raichle, 1994, Practice-related changes in human brain functional anatomy during nonmotor learning, Cereb. Cortex source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The sensorimotor striatum may be needed for the performance of habit-like behaviors and/or for the transition from goal-directed to habit-like performance.

    “These results suggest that the sensorimotor striatum may be needed a) for the performance of habit-like behaviors and/or b) for the transition from goal-directed to habit-like performance.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Automaticity and habit learning involve a shift from goal-directed action to stimulus-response behavior.

  • May combine two claims.

    Premisecitation

    Many aspects of drug-seeking behaviors become automatized, complicating treatment of drug addiction.

    “For example, a complicating factor in treating drug addiction is that many aspects of drug-seeking behaviors become automatized [79–82].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [79] Hyman, 2006, Neural mechanisms of addiction: The role of reward-related learning and memory, Annu. Rev. Neurosci. source

      Not checked in the free run.

    • cites [80] Everitt, 2008, Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction, Philos. Trans. R. Soc. Lond. B Biol. Sci. source

      Not checked in the free run.

    • cites [81] Gerdeman, 2003, It could be habit forming: Drugs of abuse and synaptic plasticity, Trends Neurosci. source

      Not checked in the free run.

    • cites [82] Canales, 2005, Stimulant-induced adaptations in neostriatal matrix and striosome systems: Transiting from instrumental responding to habitual behavior in drug addiction, Neurobiol. Learn. Mem. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    It is unknown whether the two sets of criteria would identify the same or different behaviors.

    “Thus, it is unknown whether the two sets of criteria would identify the same or different behaviors.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Striatal activation tends to disinhibit the thalamus, which tends to increase activation in targeted regions of cortex.

    “Thus, striatal activation tends to disinhibit the thalamus, which tends to increase activation in targeted regions of cortex.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The shift from goal-directed to habit behavior may be continuous rather than discrete.

    “If so, then the shift from “goal-directed” to “habit” behavior may be continuous rather than discrete.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationnone given

    Mechanisms of cortico-striatal LTP and LTD may explain the gradual reduction in the number of striatal neurons that show task-related activation over the course of training, but they do not seem to predict a shift in control from the associative to the sensorimotor striatum.

    “Mechanisms of cortico-striatal LTP and LTD (as described here) may explain the gradual reduction in the number of striatal neurons that show task-related activation over the course of training, but they do not seem to predict a shift in control from the associative to the sensorimotor striatum.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Premisenone given

    There are no systematic attempts to compare the different automaticity and habit criteria, nor examples where both sets of criteria were used in the same study.

    “We know of no systematic attempts to compare the different criteria, or even any examples where both sets of criteria were used in the same study.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).

    Premisecitation

    The basal ganglia are topographically segregated into a set of parallel loops from cortex, through the basal ganglia, and back to the originating area of cortex via the thalamus.

    “A widely-held view is that the basal ganglia are topographically segregated into a set of parallel loops from cortex, through the basal ganglia, and back to the originating area of cortex via the thalamus [25, 85].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [25] Kelly, 2004, Macro-architecture of basal ganglia loops with the cerebral cortex: Use of rabies virus to reveal multisynaptic circuits, Prog. Brain Res.

      Not checked in the free run.

    • cites [85] Alexander, 1986, Parallel organization of functionally segregated circuits linking basal ganglia and cortex, Annu. Rev. Neurosci. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The Ashby et al. model accounts for results showing that automatic behaviors are striatum- and dopamine-independent, but it does not account for results showing activation of sensorimotor striatum after automaticity has developed.

    “are striatum- and dopamine-independent, but it does not account for the results reviewed earlier showing activation of sensorimotor striatum after automaticity has developed.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [48] Ashby, 2007, A neurobiological theory of automaticity in perceptual categorization, Psychol. Rev. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    The development of automaticity is characterized by changes in widely distributed neural networks rather than in a single brain region.

    “Theoretically, the problem is difficult because the development of automaticity is characterized by changes in widely distributed neural networks, rather than in some single brain region.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    Sensorimotor regions of GPi receive inputs from sensorimotor regions of striatum and project eventually to motor/sensorimotor areas of cortex.

    “Thus, for example, sensorimotor regions of GPi receive inputs from sensorimotor regions of striatum, and project eventually to motor/sensorimotor areas of cortex.”
    Quote in the paperNot a substantial claim
19 of 19

  • The paper relies on this without support.

    Automaticity and habit learning involve a shift from goal-directed action to stimulus-response behavior.

    “As described in Box 1, habit learning is thought to involve a shift from goal-directed action to behavior that is automatically elicited by an environmental stimulus to which it has become strongly tied.”

  • The paper relies on this without support.

    The bird homologue of the basal ganglia is functionally comparable to the mammalian basal ganglia for song learning and expression.

    “Several studies have shown that disconnecting the bird homologue of the basal ganglia completely blocks new song learning, but has little effect on the expression of well-learned songs (see [31] for a review).”

  • The paper relies on this without support.

    The cited animal and human studies' measures of habit and automaticity are valid indicators of the same constructs across tasks.

    “Instead, our focus is on cortical and basal ganglia contributions to habit learning and automaticity in simple motor and cognitive tasks.”

  • The paper relies on this without support.

    Many sensory association areas of cortex project directly into premotor cortex.

    “Many sensory association areas of cortex project directly into premotor cortex.”

  • The paper relies on this without support.

    The vmPFC sends excitatory projections to the patch compartments of the striatum, which inhibits dopamine-producing cells.

    “This cortical region sends excitatory projections to the patch compartments of the striatum, which inhibits dopamine producing cells”

  • The paper relies on this without support.

    The striatum receives massive and highly convergent input from almost all of cortex.

    “The striatum receives massive and highly convergent input from almost all of cortex.”
6 of 6

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References 95 · Cited by 481

Research works printed but not linked: 1

  1. Lashley, K.S. (1950) In search of the engram. In Society of Experimental Biology Symposium (Vol. 4), pp. 454–480, Cambridge University Press

Authors
Ashby, F. G., Turner, B. O., & Horvitz, J. C.
Affiliations
  • University of California, Santa Barbara (US)
  • City College of New York (US)
Corresponding author
Ashby, F. Gregory
ORCID
Venue
Trends in Cognitive Sciences
Publisher
Elsevier BV
Published
2010-05
Volume
14
Issue
5
Pages
208-215
ISSN
1364-6613 (ISSN-L)
DOI
10.1016/j.tics.2010.02.001
PMC
PMC2862890
OpenAlex
W2128238934
Semantic Scholar
dfa61be0573cca096caa0457f285d1de39e5a4b6
Cited by
481
References
95
Citations by year
2026: 19 · 2025: 25 · 2024: 29 · 2023: 28 · 2022: 29 · 2021: 23 · 2020: 47 · 2019: 31 · 2018: 29 · 2017: 35 · 2016: 32 · 2015: 29 · 2014: 29 · 2013: 35 · 2012: 28
FWCI
2.23
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Trends in Cognitive Sciences (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (R01MH063760, R01 MH3760-2)
  • National Institute on Drug Abuse (R01DA023641)
  • Army Research Office
  • Institute for Collaborative Biotechnologies
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
habit learning, automaticity, basal ganglia, striatum, sensorimotor striatum, associative striatum, cortical control, dopamine, motor learning
MeSH terms
Association Learning, Automatism, Basal Ganglia, Cerebral Cortex, Habits, Humans, Learning

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