SHANK3 controls maturation of social reward circuits in the VTA
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Haploinsufficiency of SHANK3, encoding the synapse scaffolding protein SHANK3, leads to a highly penetrant form of autism spectrum disorder. How SHANK3 insufficiency affects specific neural circuits and how this is related to specific symptoms remains elusive. Here we used shRNA to model Shank3 insufficiency in the ventral tegmental area of mice. We identified dopamine (DA) and GABA cell-type-specific changes in excitatory synapse transmission that converge to reduce DA neuron activity and generate behavioral deficits, including impaired social preference. Administration of a positive allosteric modulator of the type 1 metabotropic glutamate receptors mGluR1 during the first postnatal week restored DA neuron excitatory synapse transmission and partially rescued the social preference defects, while optogenetic DA neuron stimulation was sufficient to enhance social preference. Collectively, these data reveal the contribution of impaired ventral tegmental area function to social behaviors and identify mGluR1 modulation during postnatal development as a potential treatment strategy.
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In mice, both congenital knockout and haploinsufficiency of Shank3 lead to diminished social interest in others and are associated with disruption of cortical and subcortical circuits thought to be involved in ASD and its ontogenesis.
“In mice, both congenital knockout and haploinsufficiency of Shank3 leads to diminished social interest in others and is associated with the disruption of cortical and subcortical circuits thought to be involved in ASD 22–26 and its ontogenesis 22,25,27,28.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [23]
Dopaminergic (DA) neurons in the lateral VTA were identified using the following criteria: firing frequency 1-5 Hz and spike width >1 ms in cell-attached configuration, membrane capacitance >28 pF, and presence of an Ih current and a leak current >150 pA when hyperpolarized from −40 mV to −120 mV in 10 mV steps.
“Dopaminergic (DA) neurons in this area were identified evaluating the following features: 1) cells firing at a frequency of 1-5 Hz and the spike width > 1ms in cell attached configuration, 2) membrane capacitance (Cm) > 28 pF and 3) the presence of an Ih current and a leak current > 150 pA, when hyperpolarized from −40 mV to −120 in 10 mV steps (Bariselli et al., 2016; Zhang et al., 2010).”
From Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder (2019) · cites this paper as Bariselli et al., 2016
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Shedding Light on Social Reward Circuitry: (Un)common Blueprints in Humans and Rodents
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Oxytocin, GABA, and dopamine interplay in autism
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Self-citation
- Authors
- Bariselli, S., Tzanoulinou, S., Glangetas, C., Prévost-Solié, C., Pucci, L., Viguié, J., Bezzi, P., O'Connor, E. C., Georges, F., Lüscher, C., & Bellone, C.
- Affiliations
- University of Lausanne (CH)
- Centre National de la Recherche Scientifique (FR)
- University of Geneva (CH)
- Corresponding author
- Bellone, Camilla
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2016-06-06
- Volume
- 19
- Issue
- 7
- Pages
- 926-934
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4948673
- OpenAlex
- W2409899008
- Cited by
- 168
- References
- 53
- Citations by year
- 2026: 9 · 2025: 16 · 2024: 15 · 2023: 24 · 2022: 24 · 2021: 25 · 2020: 12 · 2019: 9 · 2018: 20 · 2017: 12 · 2016: 2
- FWCI
- 11.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Archive ouverte UNIGE (University of Geneva) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, other-oa)
- IRIS (submittedVersion)
- HAL (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, other-oa)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
- Uni Genf
- Funders
- National Science Foundation
- Simons Foundation Autism Research Initiative
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (239496)
- Fondation Pierre Mercier
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- SHANK3, ventral tegmental area, social preferences, autism spectrum disorder, dopaminergic neurons, GABAergic neurons, metabotropic glutamate receptor 1, postnatal development, optogenetic stimulation, social behavior deficits
- MeSH terms
- Autism Spectrum Disorder, Animals, Behavior, Animal, Dopamine, Hippocampus, Mice, Inbred C57BL, Mice, Transgenic, Microfilament Proteins, Nerve Tissue Proteins, Synaptic Transmission, Reward, Synapses, Ventral Tegmental Area, Patch-Clamp Techniques, Inhibitory Postsynaptic Potentials, Dopaminergic Neurons, GABAergic Neurons
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