Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation
Open accessAbstract
Insular cortex (IC) contributes to a variety of complex brain functions, such as communication, social behavior, and self-awareness through the integration of sensory, emotional, and cognitive content. How the IC acquires its integrative properties remains unexplored. We compared the emergence of multisensory integration (MSI) in the IC of behaviorally distinct mouse strains. While adult C57BL/6 mice exhibited robust MSI, this capacity was impaired in the inbred BTBR T+tf/J mouse model of idiopathic autism. The deficit reflected weakened γ-aminobutyric acid (GABA) circuits and compromised postnatal pruning of cross-modal input. Transient pharmacological enhancement by diazepam in BTBR mice during an early sensitive period rescued inhibition and integration in the adult IC. Moreover, impaired MSI was common across three other monogenic models (GAD65, Shank3, and Mecp2 knockout mice) displaying behavioral phenotypes and parvalbumin-circuit abnormalities. Our findings offer developmental insight into a key neural circuit relevant to neuropsychiatric conditions like schizophrenia and autism.
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A decrease in PV staining intensity and puncta density of PV-ir neurons contacting pyramidal cells in the mouse insular cortex has been reported in Shank3B-/- mice.
“a decrease in PV staining intensity and puncta density of PV-ir neurons contacting pyramidal cells in the mouse insular cortex has been reported in Shank3B-/- mice [76].”
The enfeebled GABAergic circuit function reported in Shank3B-/- and Shank1-/- mice is likely to decrease somatic Ca2+ signals and subsequently modify the Ca2+ signaling components of Pvalb neurons.
“The enfeebled GABAergic circuit function reported in Shank3B-/- [76] and Shank1-/- mice [96] is likely to decrease somatic Ca2+ signals and subsequently modify the Ca2+ signaling components of Pvalb neurons”
A further link exists between Shank protein expression and Pvalb neurons.
“A further link exists between Shank protein expression and Pvalb neurons [76, 96].”
In Shank3 knockout mice, a reduction in PV+ puncta staining (intensity and puncta numbers) around pyramidal cells in the insular cortex of Shank3B-/- mice was associated with weakened GABAergic circuit function and impaired postnatal pruning.
“In Shank3 knockout mice, a reduction in PV+ puncta staining (intensity and puncta numbers) around pyramidal cells in the insular cortex of Shank3B-/- mice was associated with weakened GABAergic circuit function and impaired postnatal pruning [76].”
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- Authors
- Gogolla, N., Takesian, A. E., Feng, G., Fagiolini, M., & Hensch, T. K.
- Affiliations
- Harvard University (US)
- Canadian Institute for Advanced Research (CA)
- McGovern Institute for Brain Research (US)
- Boston Children's Hospital (US)
- Corresponding author
- Hensch, Takao K.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 83
- Issue
- 4
- Pages
- 894-905
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4177076
- OpenAlex
- W2048168580
- Cited by
- 310
- References
- 71
- Citations by year
- 2026: 14 · 2025: 22 · 2024: 14 · 2023: 33 · 2022: 37 · 2021: 24 · 2020: 30 · 2019: 26 · 2018: 27 · 2017: 31 · 2016: 26 · 2015: 23 · 2014: 3
- FWCI
- 38.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- National Institutes of Health (DP1OD003699)
- National Institute of Mental Health (P50MH094271)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- insula, multisensory integration, GABAergic circuits, BTBR T+tf/J mice, autism spectrum disorder, diazepam, parvalbumin interneurons, SHANK3, MeCP2, GAD65, schizophrenia, mouse strain differences
- MeSH terms
- Animals, Autistic Disorder, Cerebral Cortex, Diazepam, Disease Models, Animal, Glutamate Decarboxylase, Male, Microfilament Proteins, Nerve Tissue Proteins, Neural Pathways, Sensation, Species Specificity, Mice, Knockout, Mice, Methyl-CpG-Binding Protein 2, GABAergic Neurons
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