Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors
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In humans, neuroligin-3 mutations are associated with autism, whereas in mice, the corresponding mutations produce robust synaptic and behavioral changes. However, different neuroligin-3 mutations cause largely distinct phenotypes in mice, and no causal relationship links a specific synaptic dysfunction to a behavioral change. Using rotarod motor learning as a proxy for acquired repetitive behaviors in mice, we found that different neuroligin-3 mutations uniformly enhanced formation of repetitive motor routines. Surprisingly, neuroligin-3 mutations caused this phenotype not via changes in the cerebellum or dorsal striatum but via a selective synaptic impairment in the nucleus accumbens/ventral striatum. Here, neuroligin-3 mutations increased rotarod learning by specifically impeding synaptic inhibition onto D1-dopamine receptor-expressing but not D2-dopamine receptor-expressing medium spiny neurons. Our data thus suggest that different autism-associated neuroligin-3 mutations cause a common increase in acquired repetitive behaviors by impairing a specific striatal synapse and thereby provide a plausible circuit substrate for autism pathophysiology.
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Abnormal physiological feedback would affect different circuits in varying ways depending on their cellular and synaptic makeup.
“Thus, abnormal physiological feedback would affect different circuits in varying ways, depending on their cellular and synaptic makeup (Rothwell et al., 2014).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Rothwell et al., 2014
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- Authors
- Rothwell, P. E., Fuccillo, M. V., Maxeiner, S., Hayton, S. J., Gokce, O., Lim, B. K., Fowler, S. C., Malenka, R. C., & Südhof, T. C.
- Affiliations
- Stanford Medicine (US)
- University of Kansas (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Malenka, Robert C.
- Südhof, Thomas C.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 158
- Issue
- 1
- Pages
- 198-212
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4120877
- OpenAlex
- W2057250808
- Cited by
- 477
- References
- 96
- Citations by year
- 2026: 28 · 2025: 33 · 2024: 41 · 2023: 33 · 2022: 48 · 2021: 45 · 2020: 46 · 2019: 36 · 2018: 36 · 2017: 47 · 2016: 32 · 2015: 45 · 2014: 7
- FWCI
- 28.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- KU ScholarWorks (The University of Kansas) (submittedVersion, other-oa)
- Funders
- Howard Hughes Medical Institute
- Simons Foundation
- National Institute of Mental Health (F32MH096491, P50MH086403, K99MH099243)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuroligin-3, autism spectrum disorder, repetitive behavior, nucleus accumbens, ventral striatum, medium spiny neurons, dopamine D1 receptor, dopamine D2 receptor, synaptic inhibition, striatal circuits, mouse models of autism, synaptic dysfunction
- MeSH terms
- Animals, Autistic Disorder, Basal Ganglia, Humans, Membrane Proteins, Mutation, Nerve Tissue Proteins, Nucleus Accumbens, Cell Adhesion Molecules, Neuronal, Mice, Knockout, Rotarod Performance Test, Mice
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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