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Repeated Cortico-Striatal Stimulation Generates Persistent OCD-Like Behavior
Open accessAbstract
What Causes Obsessive Compulsive Disorder?: Obsessive compulsive disorder is a severe, chronic mental illness that affects millions of individuals. However, the mechanisms underlying this disease are still largely unknown (see the Perspective by Rauch and Carlezon Jr. ). Ahmari et al. (p. 1234 ) stimulated glutamatergic pathways between the orbitofrontal cortex and the ventromedial striatum and used grooming to assess obsessive compulsive behavior in mice. Repetitive stimulation over days triggered changes in the neuronal responses of the ventromedial striatum. Over time, the behavior of the animals became independent of stimulation and could be prevented by the antidepressant fluoxetine. Burguière et al. (p. 1243 ) investigated the neural basis of obsessive compulsive symptoms in a mutant mouse that showed excessive expression of a conditioned form of grooming.
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“Accumulating evidence from animal and clinical research has shown that hyperactivity in the OFC-striatum pathway plays a pivotal role in the pathology of compulsivity64–66.”
From Dissociable roles of prefrontal plasticity in decision-making strategy and execution of habitual behavior (2026) · cites this paper as [64]
In the citing paper
“While acute stimulation did not generate repetitive behaviors, repeated hyperactivation for multiple days in a row led to a progressive and persistent increase in grooming that correlated with an increased evoked-firing rate at OFC-VMS synapses.”
From DISSECTING OCD CIRCUITS: FROM ANIMAL MODELS TO TARGETED TREATMENTS: Review: Dissecting OCD Circuits: Animals to Treatments (2015) · cites this paper as [105]
In the citing paper
“Increased grooming and evoked firing were both reversed by chronic fluoxetine treatment.”
From DISSECTING OCD CIRCUITS: FROM ANIMAL MODELS TO TARGETED TREATMENTS: Review: Dissecting OCD Circuits: Animals to Treatments (2015) · cites this paper as [105]
In the citing paper
“Brief, repeated, optogenetic stimulation of mOFC terminals in VS progressively led to the development of repetitive grooming behavior that may be relevant to OCD (Ahmari et al., 2013).”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Ahmari et al., 2013
In the citing paper
“While these findings demonstrate that a circuit-level manipulation of OFC-VS projections produces OCD-like behaviors in mice (Ahmari et al., 2013)”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Ahmari et al., 2013
In the citing paper
“Together, these data suggest that abnormal functional connectivity in this interregional connection could underlie pathological repetitive behaviors (Ahmari et al., 2013).”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Ahmari et al., 2013
In the citing paper
“Moreover, they found that both grooming behaviour and the hyperactivity induced through chronic optogenetic stimulation were remediated using a common treatment for OCD, the selective-serotonin reuptake inhibitor fluoxetine (Ahmari et al., 2013).”
From The role of habit in compulsivity (2016) · cites this paper as Ahmari et al., 2013
In the citing paper
“They found that a causal relationship between this hyperactivity and the onset of compulsive grooming behaviour in otherwise healthy mice.”
From The role of habit in compulsivity (2016) · cites this paper as Ahmari et al., 2013
In the citing paper
“Compulsive grooming can be induced by optogenetically increasing medial/ventral OFC-to-DS pathway activity [49].”
From Projection-specific deficits in synaptic transmission in adult Sapap3-knockout mice (2020) · cites this paper as [49]
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“Additionally, Ahmari et al. (2013) reported that repeated stimulation of the OFC–ventromedial striatum (VMS) projections in mice using optogenetics increased the firing of postsynaptic VMS cells and the frequency of overgrooming behavior, which represents OCD symptoms in mice.”
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“Striatal overactivation has previously been associated with elevated grooming and alterations in grooming syntax (46, 62), and optogenetic stimulation of afferents to the striatum can bidirectionally modulate grooming (29, 63).”
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“Nonetheless, the increase in corticostriatal transmission could contribute to alterations of both glutamatergic (43) and dopaminergic (44) synaptic transmission.”
BackgroundMultivariate pattern analysis of obsessive–compulsive disorder using structural neuroanatomy
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“, 2013), and studies in mice have shown that repeated episodes of abnormal activity in the fronto-striatal circuit may be linked with a mechanism of persistent psychopathology in OCD (Ahmari et al., 2013).”
Interfacing behavioral and neural circuit models for habit formation
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“…in common (Peça et al., 2011; Shmelkov et al., 2010; Welch et al., 2007), and overgrooming can be induced by repetitive corticostriatal stimulation (Ahmari et al., 2013) perhaps by engaging endocannabinoid-dependent long-term depression mechanisms important for the development of habitual…”
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“Optogenetically driving cortico-striatal projections suppresses pathological grooming in a model of obsessive compulsive disorder [41], whereas activation of cortico-striatal projections at frequencies known to induce an LTD cause pathological grooming in wild-type mice [42].”
BackgroundModeling tics in rodents: Conceptual challenges and paths forward
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Projection-specific deficits in synaptic transmission in adult Sapap3-knockout mice
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“Hyperactivity in lateral orbitofrontal pathways is also strongly associated with OCD, and with compulsivity in general (Ahmari et al., 2013; Beucke et al., 2013).”
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“Despite the link of striatal dysfunction to the increased grooming behavior, it is the stimulation of corticostriatal circuit (orbitofrontal cortex to ventromedial striatum) that is required for inducing increased grooming [43].”
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Self-citationOrganization of the Anterior Limb of the Internal Capsule in the Rat
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“Rodent models using HFS of the homologs of these targets are essential for testing the mechanisms of DBS (McCracken and Grace, 2007; Mundt et al., 2009; Rodriguez-Romaguera et al., 2012; Ahmari et al., 2013; Burguière et al., 2013; Hamani et al., 2014; Rea et al., 2014).”
MethodDichotomous parvalbumin interneuron populations in dorsolateral and dorsomedial striatum
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“Thus, the repeated stimulations established a mice model with OCD-like excessive selfgrooming, as previously reported (25).”
BackgroundInfluentialHyperactivity of indirect pathway-projecting spiny projection neurons promotes compulsive behavior
Piantadosi, S. C., Manning, E. E., Chamberlain, B. L., Hyde, J., LaPalombara, Z., Bannon, N. M., Pierson, J. L., Namboodiri, V. M. K., & Ahmari, S. E. (2024) · Nature Communications · doi:10.1038/s41467-024-48331-z · Cited by 42
“Chronic fl uoxetine treatment is associated with a reduction in striatopallidal SPN hyperactivity SRIs are ef fi cacious for treating OCD in humans 52 – 55 and reducing compulsive behaviors in mouse models 11,56,57 , including compulsive grooming in Sapap3 -KO mice 33 .”
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ResultGambling disorder: an integrative review of animal and human studies
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The Psychopharmacology of Obsessive-Compulsive Disorder: A Preclinical Roadmap
Szechtman, H., Harvey, B. H., Woody, E. Z., & Hoffman, K. L. (2019) · Pharmacological Reviews · doi:10.1124/pr.119.017772 · Cited by 41
“…effects on the display of OCD-like behaviors (e.g., Campbell et al., 1999; Winter et al., 2008; Klavir et al., 2009; Dvorkin et al., 2010; Yang and Lu, 2011; Ahmari et al., 2013; Ballester González et al., 2015; Burton, 2017; Sun et al., 2019), consistent with current neuroanatomical models of OCD.”
ResultNeuromodulation of OCD: a review of invasive and non-invasive methods
Kammen, A., Cavaleri, J., Lam, J., Frank, A. C., Mason, X., Choi, W., Penn, M., Brasfield, K., Van Noppen, B., Murray, S. B., et al. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.909264 · Cited by 38
Nagarajan, N., & Capecchi, M. R. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02019-w · Cited by 41
Mouse Models of Neurodevelopmental Disease of the Basal Ganglia and Associated Circuits
Pappas, S. S., Leventhal, D., Albin, R. L., & Dauer, W. T. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-397920-9.00001-9 · Cited by 41
Treatment-refractory obsessive compulsive disorder
Atmaca, M. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.12.004 · Cited by 38
The REEP family of proteins: Molecular targets and role in pathophysiology
Fan, S., Liu, H., & Li, L. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106477 · Cited by 42
D’Antoni, C., Mautone, L., Sanchini, C., Tondo, L., Grassmann, G., Cidonio, G., Bezzi, P., Cordella, F., & Angelantonio, S. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310762 · Cited by 41
Pittenger, C. (2017) · Handbook of experimental pharmacology · doi:10.1007/164_2016_127 · Cited by 39
Marques, R. C., Vieira, L., Marques, D., & Cantilino, A. (2019) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2019-0344 · Cited by 42
Light-mediated control of Gene expression in mammalian cells
Yamada, M., Nagasaki, S. C., Ozawa, T., & Imayoshi, I. (2020) · Neuroscience Research · doi:10.1016/j.neures.2019.12.018 · Cited by 40
Manning, E. E., Wang, A. Y., Saikali, L. M., Winner, A. S., & Ahmari, S. E. (2021) · Scientific Reports · doi:10.1038/s41598-021-88769-5 · Cited by 37
Self-citationCasado-Sainz, A., Gudmundsen, F., Bærentzen, S. L., Lange, D., Ringsted, A., Tejada, I. M., Medina, S., Lee, H., Svarer, C., Keller, S. H., et al. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01207-y · Cited by 40
“Self-grooming is an innate rodent behavior characterized by a sequential pattern of movements [43], which serves as a useful proxy for compulsive behavior [24, 44, 45].”
BackgroundResultStriatal abnormalities in trichotillomania: a multi-site MRI analysis
Isobe, M., Redden, S. A., Keuthen, N. J., Stein, D. J., Lochner, C., Grant, J. E., & Chamberlain, S. R. (2018) · NeuroImage: Clinical · doi:10.1016/j.nicl.2017.12.031 · Cited by 37
“, 2005), and the striatum (playing key roles in reward processing and motor outflow) (Ahmari et al., 2013; Knutson et al., 2001).”
BackgroundKim, M., Kwak, S., Yoon, Y. B., Kwak, Y. B., Kim, T., Cho, K. I. K., Lee, T. Y., & Kwon, J. S. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0436-2 · Cited by 37
The Role of Serotonin in Orbitofrontal Function and Obsessive-Compulsive Disorder
Maia, T. V., & Cano-Colino, M. (2015) · Clinical Psychological Science · doi:10.1177/2167702614566809 · Cited by 42
“Multiple lines of evidence have suggested a central role for the OFC and associated striatal regions (particularly the caudate) in OCD (Ahmari et al., 2013; Burguière, Monteiro, Feng, & Graybiel, 2013; Evans, Lewis, & Iobst, 2004; Maia, Cooney, & Peterson, 2008; Marsh, Maia, & Peterson, 2009; Menzies et al., 2008; Rot…”
BackgroundResultInfluentialNordstrom, E. J., Bittner, K. C., McGrath, M. J., Parks, C. R., & Burton, F. H. (2015) · Brain Research · doi:10.1016/j.brainres.2015.09.032 · Cited by 37
Xu, J., Marshall, J. J., Fernandes, H. B., Nomura, T., Copits, B. A., Procissi, D., Mori, S., Wang, L., Zhu, Y., Swanson, G. T., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.073 · Cited by 37
“Prior work has demonstrated that excessive grooming in genetic or induced mouse models of OCD can be reduced by the administration of selective serotonin reuptake inhibitors (SSRIs) (Ahmari et al., 2013; Welch et al., 2007), a first line monotherapy for OCD.”
BackgroundNeuronal Glutamate Transporters Control Dopaminergic Signaling and Compulsive Behaviors
Bellini, S., Fleming, K. E., De, M., McCauley, J. P., Petroccione, M. A., D’Brant, L. Y., Tkachenko, A., Kwon, S., Jones, L. A., & Scimemi, A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1906-17.2017 · Cited by 41
“A better understanding of EAAC1 in the context of OCD is important because small changes in the excitatory drive to striatal neurons can powerfully control the activity of neuronal circuits implicated with OCD (Radulescu et al., 2017).”
InfluentialAbnormal resting-state brain activities in patients with first-episode obsessive-compulsive disorder
Niu, Q., Yang, L., Song, X., Chu, C., Liu, H., Zhang, L., Li, Y., Zhang, X., Cheng, J., & Li, Y. (2017) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s117510 · Cited by 37
Melanin concentrating hormone modulates oxytocin-mediated marble burying
Sanathara, N. M., Garau, C., Alachkar, A., Wang, L., Wang, Z., Nishimori, K., Xu, X., & Civelli, O. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.09.008 · Cited by 38
“Mice models of repetitive behavior have shown decreased activity in the lateral orbitofrontal cortex (Ahmari et al., 2013; Burguiere et al., 2013).”
BackgroundInfluentialBarahona-Corrêa, B., Camacho, M., Castro-Rodrigues, P., Costa, R. M., & Oliveira-Maia, A. J. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01798 · Cited by 37
“…modulation of orbitofrontal corticostriatal circuitry using optogenetics can induce or decrease obsessivecompulsive-like behaviors in mice (Burguière et al., 2013; Ahmari et al., 2014), and DBS of frontostriatal targets has been shown to ameliorate OCS in OCD patients (Figee et al., 2013).”
BackgroundMethodPallanti, S., Marras, A. M., Salerno, L., Makris, N., & Hollander, E. (2016) · Journal of Psychopharmacology · doi:10.1177/0269881116628427 · Cited by 36
“…with cortico-striato-thalamo-cortical (CSTC) circuitries that subserve motivation and reward-aversion, emotional learning and goal-directed action (Ahmari et al., 2013; Anticevic et al., 2014; Burguiere et al., 2013; Dougherty et al., 2010; Milad and Rauch, 2012; Pauls et al., 2014; Posner et…”
BackgroundNeuroscience: Solving the brain
Abbott, A. (2013) · Nature · doi:10.1038/499272a · Cited by 36
Kalanthroff, E., & Wheaton, M. G. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11247379 · Cited by 35
“in the cortico-striato-thalamic-cortical (CSTC) circuitry [36,37], including volumetric gray-”
BackgroundZhao, Q., Xu, T., Wang, Y., Chen, D., Liu, Q., Yang, Z., & Wang, Z. (2019) · Psychological Medicine · doi:10.1017/s0033291719002988 · Cited by 36
“The dysregulation of regions within these circuits could result in excessive reactions to threats, reduced responses to rewards, and eventually the symptoms of OCD (Ahmari et al., 2013).”
BackgroundmTORC1 in the orbitofrontal cortex promotes habitual alcohol seeking
Morisot, N., Berger, A. L., Phamluong, K., Laguesse, S., Moffat, J. J., & Dorit Ron, A. (2019) · eLife · doi:10.7554/elife.51333 · Cited by 31
“, 2016), and compulsive behaviors (Ahmari et al., 2013; Pascoli et al., 2018).”
BackgroundParolari, L., Schneeberger, M., Heintz, N., & Friedman, J. M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01162-6 · Cited by 37
Hu, X., Zhang, L., Bu, X., Li, H., Gao, Y., Lu, L., Tang, S., Wang, Y., Huang, X., & Gong, Q. (2020) · Depression and Anxiety · doi:10.1002/da.23008 · Cited by 34
‘‘Endless Stories About the Distillery’’: Joyce, Death, and Whiskey
Shovlin, F. (2007) · Fordham University Press eBooks · doi:10.1515/9781531511449-010 · Cited by 34
Timing matters: using optogenetics to chronically manipulate neural circuitry and rhythms
Sidor, M. M., & McClung, C. A. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00041 · Cited by 36
“We look forward to continued advances in the fields of electrical, mechanical, optical, and biological engineering as this will lead to a vast expansion of technological options permitting novel and more refined ways to probe the nervous system (Deisseroth and Schnitzer, 2013).”
Deep Brain Stimulation for Treatment-Refractory Mood and Obsessive-Compulsive Disorders
Widge, A. S., & Dougherty, D. D. (2015) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-015-0049-y · Cited by 32
Ho, E. V., Thompson, S. L., Katzka, W. R., Sharifi, M. F., Knowles, J. A., & Dulawa, S. C. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4086-8 · Cited by 32
“potential novel therapies (Shanahan et al. 2011; Welch et al. 2007; Ahmari et al. 2013; Shmelkov et al. 2010), and the utility of these models relies on critical validation (Geyer and Markou 1995).”
BackgroundOptogenetics: Applications in psychiatric research
Shirai, F., & Hayashi‐Takagi, A. (2017) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12516 · Cited by 33
A cross-species approach to disorders affecting brain and behaviour
Devinsky, O., Boesch, J. M., Cerdá-González, S., Coffey, B. J., Davis, K. A., Friedman, D. J., Hainline, B. W., Houpt, K. A., Lieberman, D. E., Perry, P., et al. (2018) · Nature Reviews Neurology · doi:10.1038/s41582-018-0074-z · Cited by 34
Yang, Z., Wu, G., Liu, M., Sun, X., Xu, Q., Zhang, C., & Lei, H. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.045 · Cited by 36
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Li, C., Yan, Y., Cheng, J., Xiao, G., Gu, J., Zhang, L., Yuan, S., Wang, J., Shen, Y., & Zhou, Y. (2016) · Neuroscience Bulletin · doi:10.1007/s12264-016-0015-z · Cited by 33
“Repeated corticostriatal activation generates persistent obsessive-compulsive disorder-like behavior [49].”
BackgroundCannabis Improves Obsessive-Compulsive Disorder—Case Report and Review of the Literature
Szejko, N., Fremer, C., & Müller‐Vahl, K. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00681 · Cited by 33
“Accordingly, diverse brain regions have been suggested to be affected (13, 14).”
BackgroundEffects of deep brain stimulation on prepulse inhibition in obsessive-compulsive disorder
Kohl, S., Gruendler, T. O. J., Huys, D., Sildatke, E., Dembek, T. A., Hellmich, M., Vorderwulbecke, M., Timmermann, L., Ahmari, S. E., Klosterkoetter, J., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.171 · Cited by 30
Self-citation
Metadata
- Authors
- Ahmari, S. E., Spellman, T., Douglass, N. L., Kheirbek, M. A., Simpson, H. B., Deisseroth, K., Gordon, J. A., & Hen, R.
- Affiliations
- New York State Psychiatric Institute (US)
- Columbia University Irving Medical Center (US)
- Stanford Medicine (US)
- Corresponding author
- Ahmari, Susanne E.
- ORCID
- Venue
- Science
- Published
- 2013-06-07
- Volume
- 340
- Issue
- 6137
- Pages
- 1234-1239
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3954809
- OpenAlex
- W2003956812
- Cited by
- 502
- References
- 43
- Citations by year
- 2026: 27 · 2025: 34 · 2024: 26 · 2023: 26 · 2022: 38 · 2021: 43 · 2020: 47 · 2019: 47 · 2018: 30 · 2017: 44 · 2016: 41 · 2015: 53 · 2014: 33 · 2013: 11
- FWCI
- 51.12
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (5r01mh096274-06)
- National Institute of Mental Health (K24MH091555, R01-MH096274, K01MH099371, K08MH087718)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Obsessive-Compulsive Spectrum Disorders
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- obsessive-compulsive disorder, cortico-striato-thalamo-cortical circuit, orbitofrontal cortex, ventromedial striatum, grooming, fluoxetine, optogenetics, mouse model
- MeSH terms
- Channelrhodopsins, Adenoviridae, Animals, Bacterial Proteins, Behavior, Animal, Corpus Striatum, Electric Stimulation, Fluoxetine, Frontal Lobe, Luminescent Proteins, Male, Obsessive-Compulsive Disorder, Thalamus, Selective Serotonin Reuptake Inhibitors, Artificial Gene Fusion, Mice, Optogenetics
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