Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities
Open accessAbstract
Gene mutations and gene copy number variants are associated with autism spectrum disorders (ASDs). Affected gene products are often part of signaling networks implicated in synapse formation and/or function leading to alterations in the excitation/inhibition (E/I) balance. Although the network of parvalbumin (PV)-expressing interneurons has gained particular attention in ASD, little is known on PV's putative role with respect to ASD. Genetic mouse models represent powerful translational tools for studying the role of genetic and neurobiological factors underlying ASD. Here, we report that PV knockout mice (PV(-/-)) display behavioral phenotypes with relevance to all three core symptoms present in human ASD patients: abnormal reciprocal social interactions, impairments in communication and repetitive and stereotyped patterns of behavior. PV-depleted mice also showed several signs of ASD-associated comorbidities, such as reduced pain sensitivity and startle responses yet increased seizure susceptibility, whereas no evidence for behavioral phenotypes with relevance to anxiety, depression and schizophrenia was obtained. Reduced social interactions and communication were also observed in heterozygous (PV(+/-)) mice characterized by lower PV expression levels, indicating that merely a decrease in PV levels might be sufficient to elicit core ASD-like deficits. Structural magnetic resonance imaging measurements in PV(-/-) and PV(+/-) mice further revealed ASD-associated developmental neuroanatomical changes, including transient cortical hypertrophy and cerebellar hypoplasia. Electrophysiological experiments finally demonstrated that the E/I balance in these mice is altered by modification of both inhibitory and excitatory synaptic transmission. On the basis of the reported changes in PV expression patterns in several, mostly genetic rodent models of ASD, we propose that in these models downregulation of PV might represent one of the points of convergence, thus providing a common link between apparently unrelated ASD-associated synapse structure/function phenotypes.
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Mice lacking parvalbumin have behavioral deficits, including altered social interactions.
“Moreover, mice lacking PV have behavioral deficits, including altered social interactions (Wohr et al, 2015).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Wohr et al, 2015
PV knockout mice show behavioral phenotypes resembling core autism spectrum disorder behaviors in humans.
“Concurrently, PV knockout mice display behavioral phenotypes that resemble core behavioral phenotypes found in humans with ASD [53].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [53]
Mice with reduced PV expression (PV+/-) or without PV (PV-/-) display a robust ASD-like phenotype.
“mice with reduced PV expression (PV+/-) or without PV (PV-/-) display a robust ASD-like phenotype [48]”
In striatal PV+ FSI, the increased facilitation (increased inhibition) between FSI and medium spiny neurons (MSN) caused by the absence of PV in PV-/- mice is partly compensated by a decrease in the excitatory synaptic input from cortical pyramidal cells, a mechanism hypothesized to compensate for the increased output of PV-/- neurons.
“In striatal PV+ FSI the increased facilitation (increased inhibition) between FSI and medium spiny neurons (MSN) caused by the absence of PV in PV-/-mice [53] is partly compensated by a decrease in the excitatory synaptic input from cortical pyramidal cells, a mechanism hypothesized to compensate for the increased output of PV-/- neurons [48].”
Morphological changes in PV-/- mice follow the same pattern as group 1: increased neocortical volume and decreased size of the cerebellum.
“Importantly, however, also the morphological changes in PV-/- mice follow the same pattern, as we recently demonstrated: increased neocortical volume and a decreased size of the cerebellum [48].”
Absence/down-regulation of PV in PV-/- and PV+/- mice affects the properties of Pvalb neurons and of neurons impacting on Pvalb cells, and leads to a robust ASD-like behavioral phenotype characterized by impaired social interaction behavior, reduced pro-social ultrasonic vocalizations and deficits in reversal learning.
“Absence/down-regulation of PV in PV-/- and PV+/- mice, respectively, not only affects the properties of the Pvalb neurons, but also of neurons impacting on Pvalb cells, and leads to a robust ASD-like behavioral phenotype characterized by impaired social interaction behavior, reduced pro-social ultrasonic vocalizations and deficits in reversal learning [48].”
A decrease in the number of PV+ cells has been reported in many genetic ASD mouse models in various brain regions including mPFC, SSC and striatum.
“a decrease in the number of PV+ cells has been reported in many genetic ASD mouse models in various brain regions including mPFC, SSC and striatum; (see Table S1 in [48])”
Similar neuroanatomical changes are present in PV-/- (Pvalb) mice, i.e., a transient cortical hypertrophy and a decrease in cerebellar volume at young age.
“Similar neuroanatomical changes are present in PV-/- (Pvalb) mice, i.e., a transient cortical hypertrophy and a decrease in cerebellar volume at young age [48]”
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Self-citation
- Authors
- Wöhr, M., Orduz, D., Gregory, P., Moreno, H., Khan, U., Vörckel, K. J., Wolfer, D. P., Welzl, H., Gall, D., Schiffmann, S. N., & Schwaller, B.
- Affiliations
- Philipps University of Marburg (DE)
- Université Libre de Bruxelles (BE)
- University of Fribourg (CH)
- SUNY Downstate Health Sciences University (US)
- University of Zurich (CH)
- Corresponding author
- Schwaller, B
- Venue
- Translational Psychiatry
- Published
- 2015-03-10
- Volume
- 5
- Issue
- 3
- Pages
- e525-e525
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC4354349
- OpenAlex
- W2037553020
- Cited by
- 258
- References
- 71
- Citations by year
- 2026: 16 · 2025: 18 · 2024: 20 · 2023: 20 · 2022: 23 · 2021: 24 · 2020: 39 · 2019: 24 · 2018: 28 · 2017: 20 · 2016: 16 · 2015: 10
- FWCI
- 14.82
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Translational Psychiatry (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc-sa)
- reroDoc Digital Library (submittedVersion)
- Lirias (submittedVersion, other-oa)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion, other-oa)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc-sa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc-sa)
- ETH Zürich Research Collection
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Science Foundation
- State University of New York
- Deutsche Forschungsgemeinschaft (DFG_WO1732/1-1, WO 1732/1‐1, 1732/1–1)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (241498, 130680)
- Fonds De La Recherche Scientifique - FNRS
- Fondation Médicale Reine Elisabeth
- National Institutes of Health
- SUNY Downstate Medical Center
- Neuroscience Center Zurich, University of Zurich
- National Institute on Aging (AG027476, K08AG027476)
- 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
- parvalbumin, autism spectrum disorder, social interaction deficits, communication difficulties, repetitive and stereotyped behaviors, excitation-inhibition balance, parvalbumin interneurons, cortical hypertrophy, cerebellar hypoplasia, pain sensitivity, startle response, seizure susceptibility, synaptic transmission, mouse models of autism
- MeSH terms
- Analysis of Variance, Animals, Autistic Disorder, Behavior, Animal, Brain, Disease Models, Animal, Humans, Hypertrophy, Magnetic Resonance Imaging, Male, Mice, Inbred C57BL, Neurons, Organ Size, Parvalbumins, Vocalization, Animal, Mice, Knockout, 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.
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.
What counts as a claim ›How we measure confidence ›How we check this ›
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