Common circuit defect of excitatory-inhibitory balance in mouse models of autism
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One unifying explanation for the complexity of Autism Spectrum Disorders (ASD) may lie in the disruption of excitatory/inhibitory (E/I) circuit balance during critical periods of development. We examined whether Parvalbumin (PV)-positive inhibitory neurons, which normally drive experience-dependent circuit refinement (Hensch Nat Rev Neurosci 6:877–888, 1), are disrupted across heterogeneous ASD mouse models. We performed a meta-analysis of PV expression in previously published ASD mouse models and analyzed two additional models, reflecting an embryonic chemical insult (prenatal valproate, VPA) or single-gene mutation identified in human patients (Neuroligin-3, NL-3 R451C). PV-cells were reduced in the neocortex across multiple ASD mouse models. In striking contrast to controls, both VPA and NL-3 mouse models exhibited an asymmetric PV-cell reduction across hemispheres in parietal and occipital cortices (but not the underlying area CA1). ASD mouse models may share a PV-circuit disruption, providing new insight into circuit development and potential prevention by treatment of autism.
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VPA exposure in utero leads to fewer parvalbumin-expressing interneurons in the parietal and occipital cortex, fewer glutamate decarboxylase 67-immunoreactive interneurons in the dentate gyrus, cerebellum, and cortex, and loss of motor neurons in some motor nerve nuclei in the brainstem.
“VPA exposure in utero leads to fewer parvalbumin-expressing interneurons in the parietal and occipital cortex [127], fewer glutamate decarboxylase 67-immunoreactive interneurons in the dentate gyrus, in the cerebellum and in the cortex [374], and loss of motor neurons in some of the motor nerve nuclei in the brainstem [303].”
From Autism spectrum disorder: neuropathology and animal models (2017) · cites this paper as [127]
These data are consistent with altered PV cell function in other autism mouse models.
“These data are also consistent with altered PV cell function in other autism mouse models (Gogolla et al. 2009).”
From Genetic Reduction of Matrix Metalloproteinase-9 Promotes Formation of Perineuronal Nets Around Parvalbumin-Expressing Interneurons and Normalizes Auditory Cortex Responses in Developing Fmr1 Knock-Out Mice (2018) · cites this paper as Gogolla et al. 2009
A reduction of about 20-25% in the number of PV-immunoreactive (PV+) neurons has been reported in ASD individuals and mouse ASD models.
“a reduction in the order of 20–25 % in the number of PV-immunoreactive (PV+) neurons has been reported in ASD individuals [46] and mouse ASD models [47]”
Canonical ASD mouse models were shown to display a reduction in the number of PV-immunoreactive cells in various brain regions.
“As already reported in several studies [47, 72–74] canonical ASD mouse models were shown to display a reduction in the number of PV-immunoreactive cells in various brain regions.”
Autism and schizophrenia are characterized by impaired PV-cell circuits.
“which are in turn marked by impaired PV-cell circuits (Gogolla et al., 2009; Le Magueresse and Monyer, 2013; Marin, 2012).”
From Clock Genes Control Cortical Critical Period Timing (2015) · cites this paper as Gogolla et al., 2009
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- Authors
- Gogolla, N., LeBlanc, J. J., Quast, K. B., Südhof, T. C., Fagiolini, M., & Hensch, T. K.
- Affiliations
- Harvard University (US)
- Boston Children's Hospital (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Fagiolini, Michela
- Hensch, Takao K.
- Venue
- Journal of Neurodevelopmental Disorders
- Published
- 2009-06
- Volume
- 1
- Issue
- 2
- Pages
- 172-181
- ISSN
- 1866-1947 (ISSN-L)
- 1866-1955
- PMC
- PMC2906812
- OpenAlex
- W2158463114
- Cited by
- 610
- References
- 100
- Citations by year
- 2026: 22 · 2025: 26 · 2024: 31 · 2023: 32 · 2022: 38 · 2021: 44 · 2020: 51 · 2019: 36 · 2018: 48 · 2017: 48 · 2016: 45 · 2015: 43 · 2014: 40 · 2013: 42 · 2012: 31
- FWCI
- 10.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neurodevelopmental Disorders (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Simons Foundation
- National Institute of Neurological Disorders and Stroke (R21NS062277)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- autism spectrum disorder, excitation-inhibition balance, parvalbumin interneurons, neocortex, neuroligin-3, hemispheric lateralization, circuit development, mouse models of autism, critical period
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.
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