Reduced Prefrontal Synaptic Connectivity and Disturbed Oscillatory Population Dynamics in the CNTNAP2 Model of Autism
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Abstract
Loss-of-function mutations in CNTNAP2 cause a syndromic form of autism spectrum disorder in humans and produce social deficits, repetitive behaviors, and seizures in mice. However, the functional effects of these mutations at cellular and circuit levels remain elusive. Using laser-scanning photostimulation, whole-cell recordings, and electron microscopy, we found a dramatic decrease in excitatory and inhibitory synaptic inputs onto L2/3 pyramidal neurons of the medial prefrontal cortex (mPFC) of Cntnap2 knockout (KO) mice, concurrent with reduced spines and synapses, despite normal dendritic complexity and intrinsic excitability. Moreover, recording of mPFC local field potentials (LFPs) and unit spiking in vivo revealed increased activity in inhibitory neurons, reduced phase-locking to delta and theta oscillations, and delayed phase preference during locomotion. Excitatory neurons showed similar phase modulation changes at delta frequencies. Finally, pairwise correlations increased during immobility in KO mice. Thus, reduced synaptic inputs can yield perturbed temporal coordination of neuronal firing in cortical ensembles.
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Synaptic dysfunction and excitation/inhibition imbalance is a common pathophysiological feature of multiple ASD models.
“Synaptic dysfunction and excitation/inhibition imbalance is identified as a common pathophysiological feature of multiple ASD models 137–139.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [139]
Cntnap2 KO mice exhibit a reduction in both excitatory and inhibitory synaptic inputs onto L2/3 pyramidal neurons and perturbed oscillatory activity in the mPFC.
“these mice exhibit a reduction in both excitatory and inhibitory synaptic inputs onto L2/3 pyramidal neurons and perturbed oscillatory activity in the mPFC [127].”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [127]
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- Authors
- Lazaro, M. T., Taxidis, J., Shuman, T., Bachmutsky, I., Ikrar, T., Santos, R., Marcello, G. M., Mylavarapu, A., Chandra, S., Foreman, A., Goli, R., Tran, D., Sharma, N., Azhdam, M., Dong, H., Choe, K. Y., Peñagarikano, O., Masmanidis, S. C., Rácz, B., Xu, X., Geschwind, D. H., & Golshani, P.
- Affiliations
- University of California, Los Angeles (US)
- University of California, Irvine (US)
- University of Veterinary Medicine (HU)
- University of the Basque Country (ES)
- Corresponding author
- Geschwind, Daniel H.
- Golshani, Peyman
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2019-05
- Volume
- 27
- Issue
- 9
- Pages
- 2567-2578.e6
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC6553483
- OpenAlex
- W2952701408
- Cited by
- 125
- References
- 72
- Citations by year
- 2026: 15 · 2025: 16 · 2024: 20 · 2023: 21 · 2022: 18 · 2021: 19 · 2020: 9 · 2019: 7
- FWCI
- 7.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- European Social Fund (EFOP-3.6.2-16-2017-0008)
- National Sleep Foundation
- Magyar Tudományos Akadémia (NKP-18-4)
- Epilepsy Foundation
- National Science Foundation (1707408, DGE-0707424)
- Simons Foundation (401457)
- National Institutes of Health (U54 HD87101, R01 MH105427, 1R01MH101198)
- European Commission
- Emberi Eroforrások Minisztériuma
- National Institute of Mental Health (T32MH073526, DA034178, U01 MH115746-02, P50 HD 055784-12, U01 NS094286)
- University of California, Los Angeles (5U01NS094286)
- 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
- CNTNAP2, autism spectrum disorder, medial prefrontal cortex, synaptic connectivity, pyramidal neurons, dendritic spines, inhibitory interneurons, local field potentials, neural oscillations, delta oscillations, theta oscillations, phase locking, neuronal synchronization, two-particle correlations, social dysfunction, seizures
- MeSH terms
- Animals, Autistic Disorder, Dendrites, Disease Models, Animal, Female, Male, Membrane Proteins, Mice, Inbred C57BL, Nerve Tissue Proteins, Synapses, Prefrontal Cortex, Pyramidal Cells, Mice, Knockout, Excitatory Postsynaptic Potentials, Mice
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