Dysfunction of cortical GABAergic neurons leads to sensory hyper-reactivity in a Shank3 mouse model of ASD.

Action Potentials / physiology Animals Autism Spectrum Disorder / genetics Disease Models, Animal GABAergic Neurons / physiology Mice Microfilament Proteins Nerve Tissue Proteins / genetics Physical Stimulation Pyramidal Cells / physiology Sensory Thresholds / physiology Somatosensory Cortex / physiopathology Touch / physiology Touch Perception / physiology

Journal

Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671

Informations de publication

Date de publication:
04 2020
Historique:
received: 06 08 2018
accepted: 27 01 2020
pubmed: 4 3 2020
medline: 8 7 2020
entrez: 4 3 2020
Statut: ppublish

Résumé

Hyper-reactivity to sensory input is a common and debilitating symptom in individuals with autism spectrum disorders (ASD), but the neural basis underlying sensory abnormality is not completely understood. Here we examined the neural representations of sensory perception in the neocortex of a Shank3B

Identifiants

DOI: 10.1038/s41593-020-0598-6 PMID: 32123378 PMC: PMC7131894
pubmed: 32123378
doi: 10.1038/s41593-020-0598-6
pii: 10.1038/s41593-020-0598-6
pmc: PMC7131894
mid: NIHMS1552758
doi:

Substances chimiques

Microfilament Proteins 0
Nerve Tissue Proteins 0
Shank3 protein, mouse 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

520-532

Subventions

Organisme : NIMH NIH HHS
ID : P50 MH094271
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH097104
Pays : United States
Organisme : NIMH NIH HHS
ID : R00 MH104259
Pays : United States
Organisme : NIMH NIH HHS
ID : F32 MH100749
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS045130
Pays : United States

Références

Amso, D., Haas, S., Tenenbaum, E., Markant, J. & Sheinkopf, S. J. Bottom-up attention orienting in young children with autism. J. Aut. Dev. Disord. 44, 664–673 (2014).
Leekam, S. R., Nieto, C., Libby, S. J., Wing, L. & Gould, J. Describing the sensory abnormalities of children and adults with autism. J. Aut. Dev. Disord. 37, 894–910 (2007).
Wang, A. T. et al. Neural selectivity for communicative auditory signals in Phelan-McDermid syndrome. J. Neurodev. Disord. 8, 5 (2016).
pubmed: 26909118 pmcid: 4763436
Gogolla, N., Takesian, A. E., Feng, G., Fagiolini, M. & Hensch, T. K. Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron 83, 894–905 (2014).
pubmed: 25088363 pmcid: 4177076
Goncalves, J. T., Anstey, J. E., Golshani, P. & Portera-Cailliau, C. Circuit level defects in the developing neocortex of Fragile X mice. Nat. Neurosci. 16, 903–909 (2013).
pubmed: 23727819 pmcid: 3695061
Chao, H. T. et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263–269 (2010).
pubmed: 21068835 pmcid: 3057962
Zhang, Y. et al. Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1(-/y) mice. Nat. Neurosci. 17, 1701–1709 (2014).
pubmed: 25383903
Orefice, L. L. et al. Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of ASDs. Cell 166, 299–313 (2016).
pubmed: 27293187 pmcid: 5567792
Peca, J. et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472, 437–442 (2011).
pubmed: 21423165 pmcid: 3090611
Naisbitt, S. et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23, 569–582 (1999).
pubmed: 10433268
Bozdagi, O. et al. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol. Aut. 1, 15 (2010).
Mei, Y. et al. Adult restoration of Shank3 expression rescues selective autistic-like phenotypes. Nature 530, 481–484 (2016).
pubmed: 26886798 pmcid: 4898763
Wang, X. et al. Altered mGluR5-Homer scaffolds and corticostriatal connectivity in a Shank3 complete knockout model of autism. Nat. Commun. 7, 11459 (2016).
pubmed: 27161151 pmcid: 4866051
Wang, X. et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 20, 3093–3108 (2011).
pubmed: 21558424 pmcid: 3131048
Siegle, J. H., Pritchett, D. L. & Moore, C. I. Gamma-range synchronization of fast-spiking interneurons can enhance detection of tactile stimuli. Nat. Neurosci. 17, 1371–1379 (2014).
pubmed: 25151266 pmcid: 4229565
Luo, T. Z. & Maunsell, J. H. Neuronal modulations in visual cortex are associated with only one of multiple components of attention. Neuron 86, 1182–1188 (2015).
pubmed: 26050038 pmcid: 4458699
Goel, A. et al. Impaired perceptual learning in a mouse model of Fragile X syndrome is mediated by parvalbumin neuron dysfunction and is reversible. Nat. Neurosci. 21, 1404–1411 (2018).
pubmed: 30250263 pmcid: 6161491
de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K. & Reyes, A. Correlation between neural spike trains increases with firing rate. Nature 448, 802–806 (2007).
pubmed: 17700699
Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013).
pubmed: 23868258 pmcid: 3777791
Doiron, B., Litwin-Kumar, A., Rosenbaum, R., Ocker, G. K. & Josic, K. The mechanics of state-dependent neural correlations. Nat. Neurosci. 19, 383–393 (2016).
pubmed: 26906505 pmcid: 5477791
Peron, S. P., Freeman, J., Iyer, V., Guo, C. & Svoboda, K. A cellular resolution map of barrel cortex activity during tactile behavior. Neuron 86, 783–799 (2015).
pubmed: 25913859
Crochet, S., Poulet, J. F., Kremer, Y. & Petersen, C. C. Synaptic mechanisms underlying sparse coding of active touch. Neuron 69, 1160–1175 (2011).
pubmed: 21435560
Yang, H., Kwon, S. E., Severson, K. S. & O’Connor, D. H. Origins of choice-related activity in mouse somatosensory cortex. Nat. Neurosci. 19, 127–134 (2016).
pubmed: 26642088
Kim, E. & Sheng, M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771–781 (2004).
pubmed: 15378037
Kouser, M. et al. Loss of predominant Shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission. J. Neurosci. 33, 18448–18468 (2013).
pubmed: 24259569 pmcid: 3834052
Cruikshank, S. J. et al. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813–17823 (2012).
pubmed: 23223300 pmcid: 3535493
Moore, C. I. & Nelson, S. B. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80, 2882–2892 (1998).
pubmed: 9862892
Wehr, M. & Zador, A. M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).
pubmed: 14647382
Orefice, L. L. et al. Targeting peripheral somatosensory neurons to improve tactile-related phenotypes in ASD models. Cell 178, 867–886 e824 (2019).
pubmed: 31398341
Dimidschstein, J. et al. A viral strategy for targeting and manipulating interneurons across vertebrate species. Nat. Neurosci. 19, 1743–1749 (2016).
pubmed: 27798629 pmcid: 5348112
Sachidhanandam, S., Sermet, B. S. & Petersen, C. C. H. Parvalbumin-expressing GABAergic neurons in mouse barrel cortex contribute to gating a goal-directed sensorimotor transformation. Cell Rep. 15, 700–706 (2016).
pubmed: 27149853 pmcid: 4850419
Goffin, D., Brodkin, E. S., Blendy, J. A., Siegel, S. J. & Zhou, Z. Cellular origins of auditory event-related potential deficits in Rett syndrome. Nat. Neurosci. 17, 804–806 (2014).
pubmed: 24777420 pmcid: 4038660
Selby, L., Zhang, C. & Sun, Q. Q. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci. Lett. 412, 227–232 (2007).
pubmed: 17197085
O’Neill, M. & Jones, R. S. Sensory-perceptual abnormalities in autism: a case for more research? J. Aut. Dev. Disord. 27, 283–293 (1997).
Marco, E. J., Hinkley, L. B., Hill, S. S. & Nagarajan, S. S. Sensory processing in autism: a review of neurophysiologic findings. Pediatr. Res. 69, 48R–54R (2011).
pubmed: 21289533 pmcid: 3086654
Lee, J. et al. Shank3-mutant mice lacking exon 9 show altered excitation/inhibition balance, enhanced rearing, and spatial memory deficit. Front. Cell. Neurosci. 9, 94 (2015).
pubmed: 25852484 pmcid: 4365696
Tu, J. C. et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23, 583–592 (1999).
pubmed: 10433269
Peixoto, R. T., Wang, W., Croney, D. M., Kozorovitskiy, Y. & Sabatini, B. L. Early hyperactivity and precocious maturation of corticostriatal circuits in Shank3B
pubmed: 26928064 pmcid: 4846490
Rubenstein, J. L. & Merzenich, M. M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2, 255–267 (2003).
pubmed: 14606691 pmcid: 6748642
Bolton, P. F. et al. Epilepsy in autism: features and correlates. J. Ment. Sci. 198, 289–294 (2011).
Thompson, K. J. et al. DREADD agonist 21 is an effective agonist for muscarinic-based DREADDs in vitro and in vivo. ACS Pharmacol. Transl. Sci. 1, 61–72 (2018).
pubmed: 30868140 pmcid: 6407913
Chen, Q. et al. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76, 297–308 (2012).
pubmed: 23083733 pmcid: 4059513
Truszkowski, T. L. A cellular mechanism for inverse effectiveness in multisensory integration. eLife 6, e25392 (2017).
pubmed: 28315524 pmcid: 5375642
Guizar-Sicairos, M., Thurman, S. T. & Fienup, J. R. Efficient subpixel image registration algorithms. Opt. Lett. 33, 156–158 (2008).
pubmed: 18197224
Kerlin, A. M., Andermann, M. L., Berezovskii, V. K. & Reid, R. C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67, 858–871 (2010).
pubmed: 20826316 pmcid: 3327881
Komiyama, T. et al. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464, 1182–1186 (2010).
pubmed: 20376005
Pachitariu, M., Stringer, C. & Harris, K. D. Robustness of spike deconvolution for neuronal calcium imaging. J. Neurosci. 38, 7976–7985 (2018).
pubmed: 30082416 pmcid: 6136155
Friedrich, J., Zhou, P. & Paninski, L. Fast online deconvolution of calcium imaging data. PLoS Comput. Biol. 13, e1005423 (2017).
pubmed: 28291787 pmcid: 5370160
Altman, D. G. & Bland, J. M. How to obtain the confidence interval from a P value. Brit. Med. J. 343, d2090 (2011).
pubmed: 21824904

Auteurs

Qian Chen (Q)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Christopher A Deister (CA)

Department of Neuroscience, Brown University, Providence, RI, USA.

Xian Gao (X)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.
Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Baolin Guo (B)

Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Department of Neurobiology, School of Basic Medicine, Fourth Military Medical University, Xi'an, China.

Taylor Lynn-Jones (T)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Naiyan Chen (N)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Michael F Wells (MF)

Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Runpeng Liu (R)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Michael J Goard (MJ)

Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA, USA.
Department of Psychological & Brain Sciences, University of California, Santa Barbara, Santa Barbara, CA, USA.
ORCID: 0000-0002-5366-8501

Jordane Dimidschstein (J)

Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
NYU Neuroscience Institute, New York University Langone Medical Center, New York, NY, USA.
ORCID: 0000-0001-6289-6891

Shijing Feng (S)

Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, The Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.

Yiwu Shi (Y)

Institute of Neuroscience and Department of Neurology of the Second Affiliated Hospital of Guangzhou Medical University, Key Laboratory of Neurogenetics and Channelopathies of Guangdong Province and the Ministry of Education of China, Guangzhou, China.
ORCID: 0000-0002-7962-8874

Weiping Liao (W)

Institute of Neuroscience and Department of Neurology of the Second Affiliated Hospital of Guangzhou Medical University, Key Laboratory of Neurogenetics and Channelopathies of Guangdong Province and the Ministry of Education of China, Guangzhou, China.

Zhonghua Lu (Z)

Guangdong Provincial Key Laboratory of Brain Connectome and Behavior, The Brain Cognition and Brain Disease Institute, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.

Gord Fishell (G)

Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
NYU Neuroscience Institute, New York University Langone Medical Center, New York, NY, USA.

Christopher I Moore (CI)

Department of Neuroscience, Brown University, Providence, RI, USA. Christopher_moore@brown.edu.
ORCID: 0000-0003-4534-1602

Guoping Feng (G)

McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA. fengg@mit.edu.
Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USA. fengg@mit.edu.
ORCID: 0000-0002-8021-277X

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Classifications MeSH

questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Potentiels de membrane › Potentiels d'action › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Eucaryotes › Animaux › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Troubles mentaux › Troubles du développement neurologique › Troubles généralisés du développement de l'enfant › Trouble du spectre autistique › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Techniques d'investigation › Modèles théoriques › Modèles biologiques › Modèles animaux de maladie humaine › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Cellules › Neurones › Neurones GABAergiques › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines du cytosquelette › Protéines des microfilaments › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines de tissu nerveux › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Techniques d'investigation › Stimulation physique › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Cellules › Neurones › Cellules pyramidales › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Phénomènes psychologiques › Processus mentaux › Perception › Seuils sensoriels › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Cortex sensorimoteur › Cortex somatosensoriel › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Phénomènes physiologiques de l'appareil locomoteur et du système nerveux › Phénomènes physiologiques du système nerveux › Sensation › Toucher › Dysfunction of cortical GABAergic neurons...
questionsmedicales.fr › Phénomènes psychologiques › Processus mentaux › Perception › Perception du toucher › Dysfunction of cortical GABAergic neurons...