Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

Gremel, Christina M.; Costa, Rui M.

doi:10.1038/ncomms3264

Cited by 618Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

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Gremel, Christina M., Costa, Rui M.·2013·Nature Communications

DOI 10.1038/ncomms3264PMC PMC4026062

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Abstract

Shifting between goal-directed and habitual actions allows for efficient and flexible decision making. Here we demonstrate a novel, within-subject instrumental lever-pressing paradigm, in which mice shift between goal-directed and habitual actions. We identify a role for orbitofrontal cortex (OFC) in actions following outcome revaluation, and confirm that dorsal medial (DMS) and lateral striatum (DLS) mediate different action strategies. Simultaneous in vivo recordings of OFC, DMS and DLS neuronal ensembles during shifting reveal that the same neurons display different activities depending on whether presses are goal-directed or habitual, with DMS and OFC becoming more and DLS less engaged during goal-directed actions. Importantly, the magnitude of neural activity changes in OFC following changes in outcome value positively correlates with the level of goal-directed behavior. Chemogenetic inhibition of OFC disrupts goal-directed actions, whereas optogenetic activation of OFC specifically increases goal-directed pressing. These results also reveal a role for OFC in action revaluation, which has implications for understanding compulsive behavior.

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After VR training, mice show a significant reduction in lever pressing in the devalued condition and a positive devaluation index, confirming a goal-directed strategy.
“When the devaluation test was conducted after VR training, there was a significant reduction in lever pressing in the devalued condition resulting in a positive devaluation index (1st test; Fig. 1d–f), confirming that mice employed a goal-directed strategy5,17.”
From Dissociable roles of prefrontal plasticity in decision-making strategy and execution of habitual behavior (2026) · cites this paper as [5]
The Results section ('Mice readily shift between goal-directed actions and habits'; page unavailable) reports significantly less lever pressing after devaluation in RR-trained mice and interprets that sensitivity as goal-directed behavior. The Methods section ('Statistical analyses'; page unavailable) defines an index that is positive when valued-state pressing exceeds devalued-state pressing. The source studied RR training, not the citing paper’s VR-trained mice, so it supports the interpretation but not the specific VR result. (LLM, conf=0.84)
Experimental — accuracy not yet measured
OFC's functional significance in goal-directed decision-making has been controversial; both activation and inhibition of OFC disrupt flexibility of behavior and shift it to habitual.
“In contrast to the ACC, although a number of studies implicate the OFC in reward-related decision-making, its functional significance in goal-directed decision-making has been controversial; both activation and inhibition of the OFC disrupt flexibility of a behavior and shift it to a habitual one5,44.”
From Dissociable roles of prefrontal plasticity in decision-making strategy and execution of habitual behavior (2026) · cites this paper as [5]
The Results (‘OFC conveys information about changes in action value’; page not supplied) report that OFC inhibition disrupted outcome revaluation in goal-directed mice. Activation increased pressing after devaluation in the goal-directed context, but the paper says it did not alter habitual actions; it does not establish that both manipulations shifted behavior to a habitual strategy. The Discussion (page not supplied) contrasts its finding of an OFC role in goal-directed actions with previous findings, supporting the claim that the role was contested. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Higher postsynaptic dopamine availability is associated with enhanced motor vigour, for instance speeding up reaction times, and with a very fast habitisation of behaviour.
“This can explain the empirical evidence that higher postsynaptic dopamine availability is associated with enhanced motor vigour, for instance speeding up reaction times (Berridge, 2004, Salamone and Correa, 2012), and with a very fast ‘habitisation’ of behaviour (Gremel and Costa, 2013).”
From Active Inference, homeostatic regulation and adaptive behavioural control (2015) · cites this paper as Gremel and Costa, 2013
The Results section, “Mice readily shift between goal-directed actions and habits” (page unavailable), reports that contextual cues induced mice to shift between habitual and goal-directed lever pressing. It does not establish that higher postsynaptic dopamine availability is associated with faster habit formation. The motor-vigour clause is attributed to other citations, not this paper. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Disruption of brain regions implicated in goal-directed strategy, including dorsomedial striatum, preserves reinforcement learning yet facilitates habit formation.
“Consistent with this observation, previous behavioral studies in rodents have consistently shown that disruption of brain regions implicated in goal-directed strategy, including the dorsomedial striatum, preserves reinforcement learning, yet facilitates habit formation5,40.”
From Dissociable roles of prefrontal plasticity in decision-making strategy and execution of habitual behavior (2026) · cites this paper as [5]
The caudate nucleus (dorsomedial striatum in rodents) and medial orbitofrontal cortex are important for goal-directed control over action, and the putamen is important for the gradual build-up of stimulus-response habit links over time.
“have converged on the importance of the caudate nucleus (dorsomedial striatum in rodents; DMS) and medial orbitofrontal cortex (OFC) for goal-directed control over action and the putamen for the gradual build-up of stimulus-response habit links over time.”
From The role of habit in compulsivity (2016) · cites this paper as Gremel and Costa, 2013

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Authors: Gremel, C. M., & Costa, R. M.
Affiliations: National Institutes of Health (US)
ORCID: Gremel, Christina M.
Costa, Rui M.
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2013-08-06
Volume: 4
Issue: 1
Pages: 2264-2264
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms3264
PMC: PMC4026062
OpenAlex: W2083537735
Cited by: 618
References: 62
Citations by year: 2026: 30 · 2025: 41 · 2024: 54 · 2023: 48 · 2022: 63 · 2021: 65 · 2020: 61 · 2019: 65 · 2018: 52 · 2017: 44 · 2016: 34 · 2015: 38 · 2014: 18 · 2013: 5
FWCI: 17.30
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/3.0 (unspecified)
Locations: Nature Communications (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health (Z99‐AA999999)
National Institute on Alcohol Abuse and Alcoholism
FP7 Ideas: European Research Council (243393)
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 behavior, habitual behavior, orbitofrontal cortex, dorsomedial striatum, lateral striatum, outcome value, decision-making, neuronal ensembles, chemogenetic inhibition, optogenetic stimulation, compulsive behavior, mice
MeSH terms: Animals, Behavior, Animal, Frontal Lobe, Goals, Habits, Male, Mice, Inbred C57BL, Nerve Net, Orbit, Neostriatum, Mice

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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

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