Habits are negatively regulated by histone deacetylase 3 in the dorsal striatum
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Abstract
Background Optimal behavior and decision making result from a balance of control between two strategies, one cognitive/goal-directed and one habitual. These systems are known to rely on the anatomically distinct dorsomedial and dorsolateral striatum, respectively. However, the transcriptional regulatory mechanisms required to learn and transition between these strategies are unknown. Here we examined the role of one chromatin-based transcriptional regulator, histone modification via histone deacetylases (HDACs), in this process.Methods We combined procedures that diagnose behavioral strategy in rats with pharmacological and viral-mediated HDAC manipulations, chromatin immunoprecipitation, and messenger RNA quantification.Results The results indicate that dorsal striatal HDAC3 activity constrains habit formation. Systemic HDAC inhibition following instrumental (lever press → reward) conditioning increased histone acetylation throughout the dorsal striatum and accelerated habitual control of behavior. HDAC3 was removed from the promoters of key learning-related genes in the dorsal striatum as habits formed with overtraining and with posttraining HDAC inhibition. Decreasing HDAC3 function, either by selective pharmacological inhibition or by expression of dominant-negative mutated HDAC3, in either the dorsolateral striatum or the dorsomedial striatum accelerated habit formation, while HDAC3 overexpression in either region prevented habit.Conclusions These results challenge the strict dissociation between dorsomedial striatum and dorsolateral striatum function in goal-directed versus habitual behavioral control and identify dorsostriatal HDAC3 as a critical molecular directive of the transition to habit. Because this transition is disrupted in many neurodegenerative and psychiatric diseases, these data suggest a potential molecular mechanism for the negative behavioral symptoms of these conditions and a target for therapeutic intervention.
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The striatum is involved in habit formation and goal-directed action.
“The striatum has always been suggested to be involved in habit formation and goal-directed action”
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Striatum dysfunction is an important cause of OCD.
“striatum dysfunction is an important cause of OCD (53–55)”
From Altered functional connectivity between the cerebellum and the cortico-striato-thalamo-cortical circuit in obsessive-compulsive disorder (2019) · cites this paper as [55]
Limited training on a random-interval schedule allows action-outcome learning for goal-directed decision making.
“Limited training on this regime allows action-outcome learning for goal-directed decision making41.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [41]
Group sizes were estimated based on prior work with this behavioral task and to ensure counterbalancing of virus, stress, pellet type, and devaluation test order.
“Group sizes were estimated based on prior work with this behavioral task41 and to ensure counterbalancing of virus, stress, pellet type, and devaluation test order.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [41]
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Mindfulness and Behavior Change
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Goal-directed control on interval schedules does not depend on the action–outcome correlation.
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Mercaldo, V., Vidimova, B., Gastaldo, D., Fernández, E., Lo, A. C., Cencelli, G., Pedini, G., Rubeis, S. D., Longo, F., Klann, E., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.008 · Cited by 32 · see citing works
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Coding Dynamics of the Striatal Networks During Learning
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Goal-directed actions and habits in head-fixed mice
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Epigenetics and substance use disorders: translational aspects
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Distinct but Synergistic Roles for Histone Deacetylase in the Dorsal Striatum During Habit Formation
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Maintained goal-directed control with overtraining on ratio schedulesPreprint
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Spatial interference in rats and dorsal striatum involvement in response conflict management
Poitreau, J. (2023) · theses.fr (ABES) · doi:10.70675/575f1970zc847z4b6az8583z73874d93629f
- Authors
- Malvaez, M., Greenfield, V. Y., Matheos, D. P., Angelillis, N. A., Murphy, M. D., Kennedy, P. J., Wood, M. A., & Wassum, K. M.
- Affiliations
- University of California, Los Angeles (US)
- University of California, Irvine (US)
- Corresponding author
- Wassum, Kate M.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 84
- Issue
- 5
- Pages
- 383-392
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC6082729
- OpenAlex
- W2792370189
- Cited by
- 56
- References
- 107
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 5 · 2023: 6 · 2022: 5 · 2021: 7 · 2020: 8 · 2019: 9 · 2018: 4 · 2017: 1
- FWCI
- 4.17
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- cc-by-nc-nd
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- Locations
- Biological Psychiatry (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- Hellman Foundation
- National Institute on Aging (R01AG051807)
- National Institute of Mental Health (R01MH106972)
- National Institute on Drug Abuse (F31DA023774, R01DA025922, DA 025922, DA035443, R01DA035443)
- National Institute of General Medical Sciences (R25GM055052)
- Life Sciences, University of California, Los Angeles
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
- Keywords
- HDAC3, dorsal striatum, habit formation, goal-directed behavior, operant conditioning, histone acetylation, chromatin regulation, dorsolateral striatum, dorsomedial striatum, histone deacetylase inhibition
- MeSH terms
- Histone Deacetylase 3, Animals, Conditioning, Operant, Corpus Striatum, Habits, Histone Deacetylases, Male, Neurons, Reward, Gene Expression, Rats, Long-Evans
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