Enhanced Operant Extinction and Prefrontal Excitability in a Mouse Model of Angelman Syndrome
Open accessAbstract
Angelman syndrome (AS), a neurodevelopmental disorder associated with intellectual disability, is caused by loss of maternal allele expression of UBE3A in neurons. Mouse models of AS faithfully recapitulate disease phenotypes across multiple domains, including behavior. Yet in AS, there has been only limited study of behaviors encoded by the prefrontal cortex, a region broadly involved in executive function and cognition. Because cognitive impairment is a core feature of AS, it is critical to develop behavioral readouts of prefrontal circuit function in AS mouse models. One such readout is behavioral extinction, which has been well described mechanistically and relies upon prefrontal circuits in rodents. Here we report exaggerated operant extinction in male AS model mice, concomitant with enhanced excitability in medial prefrontal neurons from male and female AS model mice. Abnormal behavior was specific to operant extinction, as two other prefrontally dependent tasks (cued fear extinction and visuospatial discrimination) were largely normal in AS model mice. Inducible deletion of Ube3a during adulthood was not sufficient to drive abnormal extinction, supporting the hypothesis that there is an early critical period for development of cognitive phenotypes in AS. This work represents the first formal experimental analysis of prefrontal circuit function in AS, and identifies operant extinction as a useful experimental paradigm for modeling cognitive aspects of AS in mice. SIGNIFICANCE STATEMENT Prefrontal cortex encodes “high-level” cognitive processes. Thus, understanding prefrontal function is critical in neurodevelopmental disorders where cognitive impairment is highly penetrant. Angelman syndrome is a neurodevelopmental disorder associated with speech and motor impairments, an outwardly happy demeanor, and intellectual disability. We describe a behavioral phenotype in a mouse model of Angelman syndrome and related abnormalities in prefrontal cortex function. We hypothesize that robust and reliable prefrontally encoded behavior may be used to model cognitive impairments in Angelman syndrome.
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Other monogenic syndromes like Kleefstra, KBG, WitKoS, Angelman, Coffin-Sirris, Rubinstein-Taybi, Phelan-McDermid, Smith-Magenis Syndrome and Kabuki syndrome also have a clear prefrontal component in their behavioral and cognitive phenotype.
“Other monogenic syndromes like Kleefstra, KBG, WitKoS, Angelman, Coffin-Sirris, Rubinstein-Taybi, Phelan-McDermid, Smith–Magenis Syndrome and Kabuki syndrome also have a clear prefrontal component in their behavioral and cognitive phenotype [272–280].”
From Development of prefrontal cortex (2022) · cites this paper as [277]
The Abstract and Discussion report exaggerated operant extinction and hyperexcitable prefrontal neurons in Angelman syndrome model mice, supporting a prefrontal component for the Angelman part of the cited list. The paper does not establish that component as clear in people with Angelman syndrome; its Introduction says prefrontal dysfunction likely contributes to cognitive impairment, and the Abstract notes that two other prefrontally dependent tasks were largely normal. (LLM, conf=0.84)
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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
- Sidorov, M. S., Judson, M. C., Kim, H., Rougie, M., Ferrer, A. I., Nikolova, V. D., Riddick, N. V., Moy, S. S., & Philpot, B. D.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-02-05
- Volume
- 38
- Issue
- 11
- Pages
- 2671-2682
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5852653
- OpenAlex
- W2787375251
- Cited by
- 25
- References
- 69
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 1 · 2022: 3 · 2021: 3 · 2020: 6 · 2019: 5
- FWCI
- 2.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS085093, F32NS077686, P30NS045892)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD079124, T32HD040127)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- Angelman syndrome, UBE3A, operant extinction, prefrontal cortex, neuronal excitability, cognitive impairment, intellectual disability, neurodevelopmental disorders, fear extinction, maternal allele expression, critical period, mouse model
- MeSH terms
- Animals, Cognition, Cognition Disorders, Conditioning, Operant, Cues, Discrimination, Psychological, Extinction, Psychological, Male, Mice, Inbred C57BL, Phenotype, Angelman Syndrome, Gene Deletion, Prefrontal Cortex, Patch-Clamp Techniques, Ubiquitin-Protein Ligases, Mice, Executive Function
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