Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action

Balleine, Bernard W; O'Doherty, John P

doi:10.1038/npp.2009.131

Cited by 1,775Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action

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Balleine, Bernard W, O'Doherty, John P·2010·Neuropsychopharmacology

DOI 10.1038/npp.2009.131PMC PMC3055420

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Abstract

Recent behavioral studies in both humans and rodents have found evidence that performance in decision-making tasks depends on two different learning processes; one encoding the relationship between actions and their consequences and a second involving the formation of stimulus-response associations. These learning processes are thought to govern goal-directed and habitual actions, respectively, and have been found to depend on homologous corticostriatal networks in these species. Thus, recent research using comparable behavioral tasks in both humans and rats has implicated homologous regions of cortex (medial prefrontal cortex/medial orbital cortex in humans and prelimbic cortex in rats) and of dorsal striatum (anterior caudate in humans and dorsomedial striatum in rats) in goal-directed action and in the control of habitual actions (posterior lateral putamen in humans and dorsolateral striatum in rats). These learning processes have been argued to be antagonistic or competing because their control over performance appears to be all or none. Nevertheless, evidence has started to accumulate suggesting that they may at times compete and at others cooperate in the selection and subsequent evaluation of actions necessary for normal choice performance. It appears likely that cooperation or competition between these sources of action control depends not only on local interactions in dorsal striatum but also on the cortico-basal ganglia network within which the striatum is embedded and that mediates the integration of learning with basic motivational and emotional processes. The neural basis of the integration of learning and motivation in choice and decision-making is still controversial and we review some recent hypotheses relating to this issue.

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Act/outcome system involves prelimbic area of vmPFC and posterior DMS; habit system involves sensorimotor cortex and DLS.
“Importantly, the act/outcome system involves a corticostriatal circuit consisting of the prelimbic area within the ventromedial prefrontal cortex and the posterior dorsal medial striatum (DMS), while the”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Balleine & O'Doherty, 2010
The Neural Substrates of Goal-Directed Learning section identifies a rat prelimbic–dorsomedial striatal circuit for goal-directed learning, and the Figure 2 caption (Future Directions) links sensorimotor cortical inputs to dorsolateral striatum with habits. The paper describes rodent prelimbic cortex as analogous to human vmPFC, not as an area within it, and the cited passages do not specify the posterior dorsomedial striatum. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Motor learning can be divided into two stages: associative learning in the early stage and skill learning in the late stage.
“Motor learning can be divided into two stages: associative learning in the early stage and skill learning in the late stage (Balleine & O'Doherty, 2010 ; Doyon & Benali, 2005 ; Makino, Hwang, Hedrick, & Komiyama, 2016 ).”
From Motor learning requires myelination to reduce asynchrony and spontaneity in neural activity (2020) · cites this paper as Balleine & O'Doherty, 2010
The Summary describes two associative processes in action learning, and Neural Substrates of Habit Learning contrasts goal-directed responding early in training with habitual responding after overtraining (page unavailable). That supports a change with training, but the paper does not divide motor learning into an early associative-learning stage and a late skill-learning stage; it describes both goal-directed and habitual learning as associative processes. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Act/outcome system is sensitive to response-reinforcer contingency; habit system is sensitive only to temporal pairing and not contingency.
“One system, called the “act/outcome” system, is sensitive to the contingency between response and reinforcer.”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Balleine & O'Doherty, 2010
The vmPFC is commonly associated with a "goal-directed" system.
“By contrast, the vmPFC, an often ill-defined area potentially comprising several distinct cytoarchitectonic regions (Fig. 2), is commonly associated with a “goal-directed” system [7].”
From The role of prefrontal cortex in cognitive control and executive function (2022) · cites this paper as [7]
Regulation of goal-directed and habitual behaviors by cortico-striatal pathways is well established.
“The regulation of goal-directed and habitual behaviors by cortico-striatal pathways is well established8,10.”
From Dissociable roles of prefrontal plasticity in decision-making strategy and execution of habitual behavior (2026) · cites this paper as [10]

Failure to detect changes in action-outcome contingencies (associated with disrupted areas 32/24 in monkeys and PLc in rodents) could contribute to negative biases in approach-avoidance decision making and despair/helplessness.
“a failure to detect changes in the contingencies between one's actions and their outcome (associated with disrupted function in both areas 32 and 24 in monkeys [206] and PLc in rodents [205,250]) could contribute not only to negative biases in approach-avoidance decision making but also despair/helplessness [232].”
From Prefrontal cortex and depression (2022) · cites this paper as [250]
The neural circuits underlying the balance between habitual and goal-directed behavior have been well defined in the neuroscience literature, overlapping with the frontostriatal circuits known to be involved in OCD.
“The neural circuits underlying the balance between habitual and goal-directed behavior have been well defined in the neuroscience literature, overlapping with the frontostriatal circuits known to be involved in OCD 25, 26, 27.”
From Enhanced avoidance habits in obsessive-compulsive disorder (2014) · cites this paper as [25]
Converging effects in a number of related paradigms have led to the idea that the OFC-vmPFC system represents expectations about specific outcomes, which perhaps provides clues as to the roots of conceptual, prospective thought.
“Converging effects in a number of related paradigms has led to the idea that the OFC-vmPFC system represents expectations about specific outcomes [15,20], which perhaps provides clues as to the roots of conceptual, prospective thought.”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [20]
The view of affective meaning aligns with dual-process views in which model-based or goal-directed systems operate alongside simpler habit-learning systems to guide reward-driven learning in animals.
“and with other dual-process views that suggest that ‘model-based’ or ‘goal-directed’ systems operate alongside simpler habit learning systems to guide reward-driven learning in animals [20,43].”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [20]
Instead of erasing R-O, S-R exists along with it, coded by a separate circuit in the brain.
“However, instead of erasing R-O, S-R exists along with it, coded by a separate circuit in the brain (e.g., Balleine, 2019; Balleine & O'Doherty, 2010; Gruber & McDonald, 2012; Robbins et al., 2019).”
From Context, attention, and the switch between habit and goal-direction in behavior (2021) · cites this paper as Balleine & O'Doherty, 2010
The dorsomedial striatum is an evolutionarily conserved hub for the action-outcome learning that supports goal-directed decision making.
“The dorsomedial striatum (DMS) is an evolutionarily conserved hub for the action-outcome learning that supports goal-directed decision making26,27.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [27]
Suppression of DMS neuronal activity promotes inflexible habits.
“DMS neuronal activity, especially plasticity in dopamine D1 receptor-expressing neurons72, is critical for the action-outcome learning that supports goal-directed decision making and when suppressed promotes inflexible habits26–28.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [27]
Striatal regions support dissociable associative learning strategies that may respectively dominate at various stages of training, depending on the task.
“a more parsimonious interpretation is that striatal regions support dissociable associative learning strategies that may respectively dominate at various stages of training, depending on the task [3,50,51].”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [50]
Premotor or prefrontal cortical areas directly interact with the dorsal striatum and have been shown to actively compute higher-order variables such as environmental uncertainty and cognitive effort.
“The potentially higher-level nature points to regions such as premotor or prefrontal cortical areas3,72, which directly interact with the dorsal striatum73, and have been shown to actively compute higher-order variables such as environmental uncertainty and cognitive effort3,72–79.”
From Revealing abrupt transitions from goal-directed to habitual behavior (2026) · cites this paper as [73]

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[58]58. Dickinson A (1994). Instrumental conditioning. In: Mackintosh NJ (ed). Animal Cognition and Learning. Academic Press: London. pp 4-79. An important review that evaluates experimental evidence for and against a variety of theories of instrumental conditioning.

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Authors: Balleine, B. W., & O'Doherty, J. P.
Affiliations: The University of Sydney (AU)
Corresponding author: Balleine, Bernard W
ORCID: Balleine, Bernard W
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2009-09-23
Volume: 35
Issue: 1
Pages: 48-69
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/npp.2009.131
PMC: PMC3055420
OpenAlex: W2057001461
Semantic Scholar: a386eb224d6be2ab3f48b015ced299c3929ff0ba
Cited by: 1,775
References: 219
Citations by year: 2026: 86 · 2025: 103 · 2024: 117 · 2023: 103 · 2022: 117 · 2021: 128 · 2020: 125 · 2019: 119 · 2018: 128 · 2017: 114 · 2016: 111 · 2015: 112 · 2014: 119 · 2013: 109 · 2012: 73
FWCI: 4.26
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Funders: Science Foundation Ireland
National Institute of Neurological Disorders and Stroke
National Center for Research Resources (UL1RR024911, RR24911)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD059257, HD59257)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: goal-directed action, habitual behavior, corticostriatal circuits, dorsal striatum, medial prefrontal cortex, prelimbic cortex, dorsolateral striatum, dorsomedial striatum, action control, decision-making, learning and motivation, cortico-basal ganglia network
MeSH terms: Animals, Cerebral Cortex, Corpus Striatum, Goals, Habits, Humans, Motor Activity, Neural Pathways, Psychomotor Performance, Rats

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Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action

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