Altered synaptic ultrastructure in the prefrontal cortex of Shank3-deficient rats
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Abstract
Background: Deletion or mutations of SHANK3 lead to Phelan–McDermid syndrome and monogenic forms of autism spectrum disorder (ASD). SHANK3 encodes its eponymous scaffolding protein at excitatory glutamatergic synapses. Altered morphology of dendrites and spines in the hippocampus, cerebellum, and striatum have been associated with behavioral impairments in Shank3-deficient animal models. Given the attentional deficit in these animals, our study explored whether deficiency of Shank3 in a rat model alters neuron morphology and synaptic ultrastructure in the medial prefrontal cortex (mPFC). Methods: We assessed dendrite and spine morphology and spine density in mPFC layer III neurons in Shank3 -homozygous knockout ( Shank3 -KO), heterozygous ( Shank3 -Het), and wild-type (WT) rats. We used electron microscopy to determine the density of asymmetric synapses in mPFC layer III excitatory neurons in these rats. We measured postsynaptic density (PSD) length, PSD area, and head diameter (HD) of spines at these synapses. Results: Basal dendritic morphology was similar among the three genotypes. Spine density and morphology were comparable, but more thin and mushroom spines had larger head volumes in Shank3 -Het compared to WT and Shank3 -KO. All three groups had comparable synapse density and PSD length. Spine HD of total and non-perforated synapses in Shank3 -Het rats, but not Shank3 -KO rats, was significantly larger than in WT rats. The total and non-perforated PSD area was significantly larger in Shank3 -Het rats compared to Shank3 -KO rats. These findings represent preliminary evidence for synaptic ultrastructural alterations in the mPFC of rats that lack one copy of Shank3 and mimic the heterozygous loss of SHANK3 in Phelan–McDermid syndrome. Limitations: The Shank3 deletion in the rat model we used does not affect all isoforms of the protein and would only model the effect of mutations resulting in loss of the N-terminus of the protein. Given the higher prevalence of ASD in males, the ultrastructural study focused only on synaptic structure in male Shank3 -deficient rats. Conclusions: We observed increased HD and PSD area in Shank3 -Het rats. These observations suggest the occurrence of altered synaptic ultrastructure in this animal model, further pointing to a key role of defective expression of the Shank3 protein in ASD and Phelan–McDermid syndrome.
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For some of these monogenic syndromes it has recently been shown that deficits in the structural development of the PFC underlie these problems.
“For some of these syndromes it has recently been shown that deficits in the structural development of the PFC underlie these problems [281–287].”
From Development of prefrontal cortex (2022) · cites this paper as [284]
The Conclusions report altered synaptic ultrastructure in the medial PFC of Shank3-deficient rats and say the changes may have implications for attentional deficits. The paper does not show that disrupted PFC structural development causes those deficits; its conclusion is tentative and based on a rat model, not a demonstration across monogenic syndromes. (LLM, conf=0.86)
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Flagged first, then by citations
Cited by
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Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
- Authors
- Jacot-Descombes, S., Keshav, N. U., Dickstein, D. L., Wicinski, B., Janssen, W. G. M., Hiester, L. L., Sarfo, E. K., Warda, T., Fam, M. M., Harony-Nicolas, H., Buxbaum, J. D., Hof, P. R., & Varghese, M.
- Affiliations
- University of Geneva (CH)
- Icahn School of Medicine at Mount Sinai (US)
- Uniformed Services University of the Health Sciences (US)
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Hof, Patrick R.
- Varghese, Merina
- ORCID
- Venue
- Molecular Autism
- Published
- 2020-11-17
- Volume
- 11
- Issue
- 1
- Pages
- 89-89
- ISSN
- 2040-2392 (ISSN-L)
- PMC
- PMC7671669
- OpenAlex
- W3104429824
- Cited by
- 41
- References
- 102
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 14 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 1
- FWCI
- 2.20
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Molecular Autism (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Beatrice and Samuel A. Seaver Foundation
- Simons Foundation (345922)
- Foundation for Prader-Willi Research
- Foundation for the National Institutes of Health (MH093725, MH101584)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Keywords
- SHANK3, Phelan-McDermid syndrome, autism spectrum disorder, synaptic ultrastructure, medial prefrontal cortex, dendritic spines, postsynaptic density, dendritic spine morphology, synaptic density, mushroom spines, attention deficits, synaptic scaffolding
- MeSH terms
- Animals, Female, Heterozygote, Male, Nerve Tissue Proteins, Synapses, Prefrontal Cortex, Dendritic Spines, Rats, Post-Synaptic Density
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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