Cortical interneurons in autism.
Journal
Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
27
02
2021
accepted:
21
09
2021
entrez:
1
12
2021
pubmed:
2
12
2021
medline:
7
4
2022
Statut:
ppublish
Résumé
The mechanistic underpinnings of autism remain a subject of debate and controversy. Why do individuals with autism share an overlapping set of atypical behaviors and symptoms, despite having different genetic and environmental risk factors? A major challenge in developing new therapies for autism has been the inability to identify convergent neural phenotypes that could explain the common set of symptoms that result in the diagnosis. Although no striking macroscopic neuropathological changes have been identified in autism, there is growing evidence that inhibitory interneurons (INs) play an important role in its neural basis. In this Review, we evaluate and interpret this evidence, focusing on recent findings showing reduced density and activity of the parvalbumin class of INs. We discuss the need for additional studies that investigate how genes and the environment interact to change the developmental trajectory of INs, permanently altering their numbers, connectivity and circuit engagement.
Identifiants
pubmed: 34848882
doi: 10.1038/s41593-021-00967-6
pii: 10.1038/s41593-021-00967-6
pmc: PMC9798607
mid: NIHMS1857455
doi:
Substances chimiques
Parvalbumins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1648-1659Subventions
Organisme : NICHD NIH HHS
ID : R01 HD054453
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH099114
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS105502
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS117597
Pays : United States
Informations de copyright
© 2021. Springer Nature America, Inc.
Références
Lombardo, M. V., Lai, M. C. & Baron-Cohen, S. Big data approaches to decomposing heterogeneity across the autism spectrum. Mol. Psychiatry 24, 1435–1450 (2019).
pubmed: 30617272
pmcid: 6754748
doi: 10.1038/s41380-018-0321-0
Iakoucheva, L. M., Muotri, A. R. & Sebat, J. Getting to the cores of autism. Cell 178, 1287–1298 (2019).
pubmed: 31491383
pmcid: 7039308
doi: 10.1016/j.cell.2019.07.037
Belmonte, M. K. et al. Autism and abnormal development of brain connectivity. J. Neurosci. 24, 9228–9231 (2004).
pubmed: 15496656
pmcid: 6730085
doi: 10.1523/JNEUROSCI.3340-04.2004
Hussman, J. P. Suppressed GABAergic inhibition as a common factor in suspected etiologies of autism. J. Autism Dev. Disord. 31, 247–248 (2001).
pubmed: 11450824
doi: 10.1023/A:1010715619091
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
doi: 10.1034/j.1601-183X.2003.00037.x
Jeste, S. S. & Tuchman, R. Autism spectrum disorder and epilepsy: two sides of the same coin? J. Child Neurol. 30, 1963–1971 (2015).
pubmed: 26374786
pmcid: 4648708
doi: 10.1177/0883073815601501
Pan, P. Y., Bolte, S., Kaur, P., Jamil, S. & Jonsson, U. Neurological disorders in autism: a systematic review and meta-analysis. Autism 25, 812–830 (2021).
pubmed: 32907344
doi: 10.1177/1362361320951370
O’Donnell, C., Goncalves, J. T., Portera-Cailliau, C. & Sejnowski, T. J. Beyond excitation/inhibition imbalance in multidimensional models of neural circuit changes in brain disorders. Elife 6, e26724 (2017).
Marin, O. Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107–120 (2012).
pubmed: 22251963
doi: 10.1038/nrn3155
Ferguson, B. R. & Gao, W. J. PV Interneurons: critical regulators of E/I balance for prefrontal cortex-dependent behavior and psychiatric disorders. Front. Neural Circuits 12, 37 (2018).
pubmed: 29867371
pmcid: 5964203
doi: 10.3389/fncir.2018.00037
Filice, F., Janickova, L., Henzi, T., Bilella, A. & Schwaller, B. The parvalbumin hypothesis of autism spectrum disorder. Front. Cell. Neurosci. 14, 577525 (2020).
pubmed: 33390904
pmcid: 7775315
doi: 10.3389/fncel.2020.577525
Lunden, J. W., Durens, M., Phillips, A. W. & Nestor, M. W. Cortical interneuron function in autism spectrum condition. Pediatr. Res 85, 146–154 (2019).
pubmed: 30367159
doi: 10.1038/s41390-018-0214-6
Rossignol, E. Genetics and function of neocortical GABAergic interneurons in neurodevelopmental disorders. Neural Plast. 2011, 649325 (2011).
pubmed: 21876820
pmcid: 3159129
doi: 10.1155/2011/649325
Hu, H., Gan, J. & Jonas, P. Interneurons. Fast-spiking, parvalbumin
pubmed: 25082707
doi: 10.1126/science.1255263
Gandal, M. J. et al. Shared molecular neuropathology across major psychiatric disorders parallels polygenic overlap. Science 359, 693–697 (2018).
pubmed: 29439242
pmcid: 5898828
doi: 10.1126/science.aad6469
Haney, J. R. et al. Broad transcriptomic dysregulation across the cerebral cortex in ASD. Preprint at BioRxiv https://doi.org/10.1101/2020.12.17.423129 (2020).
Williams, R. S., Hauser, S. L., Purpura, D. P., DeLong, G. R. & Swisher, C. N. Autism and mental retardation: neuropathologic studies performed in four retarded persons with autistic behavior. Arch. Neurol. 37, 749–753 (1980).
pubmed: 7447762
doi: 10.1001/archneur.1980.00500610029003
Markicevic, M. et al. Cortical excitation:inhibition imbalance causes abnormal brain network dynamics as observed in neurodevelopmental disorders. Cereb. Cortex 30, 4922–4937 (2020).
pubmed: 32313923
pmcid: 7391279
doi: 10.1093/cercor/bhaa084
Casanova, M. F., Buxhoeveden, D. P., Switala, A. E. & Roy, E. Minicolumnar pathology in autism. Neurology 58, 428–432 (2002).
pubmed: 11839843
doi: 10.1212/WNL.58.3.428
Wegiel, J. et al. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 119, 755–770 (2010).
pubmed: 20198484
pmcid: 2869041
doi: 10.1007/s00401-010-0655-4
Varghese, M. et al. Autism spectrum disorder: neuropathology and animal models. Acta Neuropathol. 134, 537–566 (2017).
pubmed: 28584888
pmcid: 5693718
doi: 10.1007/s00401-017-1736-4
Hutsler, J. J. & Zhang, H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res. 1309, 83–94 (2010).
pubmed: 19896929
doi: 10.1016/j.brainres.2009.09.120
Martinez-Cerdeño, V. Dendrite and spine modifications in autism and related neurodevelopmental disorders in patients and animal models. Dev. Neurobiol. 77, 393–404 (2017).
pubmed: 27390186
doi: 10.1002/dneu.22417
Fatemi, S. H., Reutiman, T. J., Folsom, T. D. & Thuras, P. D. GABA
pubmed: 18821008
doi: 10.1007/s10803-008-0646-7
Blatt, G. J. et al. Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J. Autism Dev. Disord. 31, 537–543 (2001).
pubmed: 11814263
doi: 10.1023/A:1013238809666
Robertson, C. E., Ratai, E. M. & Kanwisher, N. Reduced GABAergic action in the autistic brain. Curr. Biol. 26, 80–85 (2016).
pubmed: 26711497
doi: 10.1016/j.cub.2015.11.019
Horder, J. et al. GABA
Palmen, S. J., van Engeland, H., Hof, P. R. & Schmitz, C. Neuropathological findings in autism. Brain 127, 2572–2583 (2004).
pubmed: 15329353
doi: 10.1093/brain/awh287
Lawrence, Y. A., Kemper, T. L., Bauman, M. L. & Blatt, G. J. Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism. Acta Neurol. Scand. 121, 99–108 (2010).
pubmed: 19719810
doi: 10.1111/j.1600-0404.2009.01234.x
Hashemi, E., Ariza, J., Rogers, H., Noctor, S. C. & Martinez-Cerdeño, V. The number of parvalbumin-expressing interneurons is decreased in the prefrontal cortex in autism. Cereb. Cortex 27, 1931–1943 (2017).
pubmed: 26922658
Ariza, J., Rogers, H., Hashemi, E., Noctor, S. C. & Martinez-Cerdeño, V. The number of chandelier and basket cells are differentially decreased in prefrontal cortex in autism. Cereb. Cortex 28, 411–420 (2018).
pubmed: 28122807
doi: 10.1093/cercor/bhw349
Li, X. G., Somogyi, P., Tepper, J. M. & Buzsaki, G. Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Exp. Brain Res. 90, 519–525 (1992).
pubmed: 1385200
doi: 10.1007/BF00230934
Gogolla, N. et al. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J. Neurodev. Disord. 1, 172–181 (2009).
pubmed: 20664807
pmcid: 2906812
doi: 10.1007/s11689-009-9023-x
Canetta, S. et al. Maternal immune activation leads to selective functional deficits in offspring parvalbumin interneurons. Mol. Psychiatry 21, 956–968 (2016).
pubmed: 26830140
pmcid: 4914410
doi: 10.1038/mp.2015.222
Godavarthi, S. K., Sharma, A. & Jana, N. R. Reversal of reduced parvalbumin neurons in hippocampus and amygdala of Angelman syndrome model mice by chronic treatment of fluoxetine. J. Neurochem. 130, 444–454 (2014).
pubmed: 24678582
doi: 10.1111/jnc.12726
Chen, Z. et al. Accumulated quiescent neural stem cells in adult hippocampus of the mouse model for the MECP2 duplication syndrome. Sci. Rep. 7, 41701 (2017).
pubmed: 28139724
pmcid: 5282511
doi: 10.1038/srep41701
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
doi: 10.1016/j.neulet.2006.11.062
Wen, T. H. et al. Genetic reduction of matrix metalloproteinase-9 promotes formation of perineuronal nets around parvalbumin-expressing interneurons and normalizes auditory cortex responses in developing Fmr1 knock-out mice. Cereb. Cortex 28, 3951–3964 (2018).
pubmed: 29040407
doi: 10.1093/cercor/bhx258
Filice, F., Vorckel, K. J., Sungur, A. O., Wohr, M. & Schwaller, B. Reduction in parvalbumin expression not loss of the parvalbumin-expressing GABA interneuron subpopulation in genetic parvalbumin and shank mouse models of autism. Mol. Brain 9, 10 (2016).
pubmed: 26819149
pmcid: 4729132
doi: 10.1186/s13041-016-0192-8
Lauber, E., Filice, F. & Schwaller, B. Dysregulation of parvalbumin expression in the Cntnap2
pubmed: 30116174
pmcid: 6082962
doi: 10.3389/fnmol.2018.00262
Penagarikano, O. et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 147, 235–246 (2011).
pubmed: 21962519
pmcid: 3390029
doi: 10.1016/j.cell.2011.08.040
Hoffman, E. J. et al. Estrogens suppress a behavioral phenotype in zebrafish mutants of the autism risk gene, CNTNAP2. Neuron 89, 725–733 (2016).
pubmed: 26833134
pmcid: 4766582
doi: 10.1016/j.neuron.2015.12.039
Scott, R. et al. Loss of Cntnap2 causes axonal excitability deficits, developmental delay in cortical myelination, and abnormal stereotyped motor behavior. Cereb. Cortex 29, 586–597 (2019).
pubmed: 29300891
doi: 10.1093/cercor/bhx341
Smith, C. J. et al. Neonatal immune challenge induces female-specific changes in social behavior and somatostatin cell number. Brain Behav. Immun. 90, 332–345 (2020).
pubmed: 32860938
pmcid: 7556772
doi: 10.1016/j.bbi.2020.08.013
Vogt, D., Cho, K. K. A., Lee, A. T., Sohal, V. S. & Rubenstein, J. L. R. The parvalbumin/somatostatin ratio is increased in Pten mutant mice and by human PTEN ASD alleles. Cell Rep. 11, 944–956 (2015).
pubmed: 25937288
pmcid: 4431948
doi: 10.1016/j.celrep.2015.04.019
Lim, L., Mi, D., Llorca, A. & Marin, O. Development and functional diversification of cortical interneurons. Neuron 100, 294–313 (2018).
pubmed: 30359598
pmcid: 6290988
doi: 10.1016/j.neuron.2018.10.009
Paluszkiewicz, S. M., Olmos-Serrano, J. L., Corbin, J. G. & Huntsman, M. M. Impaired inhibitory control of cortical synchronization in Fragile X syndrome. J. Neurophysiol. 106, 2264–2272 (2011).
pubmed: 21795626
pmcid: 3214096
doi: 10.1152/jn.00421.2011
Wong, F. K. et al. Pyramidal cell regulation of interneuron survival sculpts cortical networks. Nature 557, 668–673 (2018).
pubmed: 29849154
pmcid: 6207348
doi: 10.1038/s41586-018-0139-6
Southwell, D. G. et al. Intrinsically determined cell death of developing cortical interneurons. Nature 491, 109–113 (2012).
pubmed: 23041929
pmcid: 3726009
doi: 10.1038/nature11523
Wong, F. K. & Marin, O. Developmental cell death in the cerebral cortex. Annu. Rev. Cell Dev. Biol. 35, 523–542 (2019).
pubmed: 31283379
doi: 10.1146/annurev-cellbio-100818-125204
Denaxa, M. et al. Modulation of apoptosis controls inhibitory interneuron number in the cortex. Cell Rep. 22, 1710–1721 (2018).
pubmed: 29444425
pmcid: 6230259
doi: 10.1016/j.celrep.2018.01.064
Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004).
pubmed: 15592414
doi: 10.1038/nature03132
Golshani, P. et al. Internally mediated developmental desynchronization of neocortical network activity. J. Neurosci. 29, 10890–10899 (2009).
pubmed: 19726647
pmcid: 2771734
doi: 10.1523/JNEUROSCI.2012-09.2009
Duan, Z. R. S. et al. GABAergic restriction of network dynamics regulates interneuron survival in the developing cortex. Neuron 105, 75–92 (2020).
pubmed: 31780329
doi: 10.1016/j.neuron.2019.10.008
del Rio, J. A., de Lecea, L., Ferrer, I. & Soriano, E. The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Brain Res. Dev. Brain Res. 81, 247–259 (1994).
pubmed: 7813046
doi: 10.1016/0165-3806(94)90311-5
Priya, R. et al. Activity regulates cell death within cortical interneurons through a calcineurin-dependent mechanism. Cell Rep. 22, 1695–1709 (2018).
pubmed: 29444424
pmcid: 6215776
doi: 10.1016/j.celrep.2018.01.007
Marin, O. Developmental timing and critical windows for the treatment of psychiatric disorders. Nat. Med. 22, 1229–1238 (2016).
pubmed: 27783067
doi: 10.1038/nm.4225
Nomura, T. et al. Delayed maturation of fast-spiking interneurons is rectified by activation of the TrkB receptor in the mouse model of Fragile X syndrome. J. Neurosci. 37, 11298–11310 (2017).
pubmed: 29038238
pmcid: 5700416
doi: 10.1523/JNEUROSCI.2893-16.2017
Petilla Interneuron Nomenclature Group, et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557–568 (2008).
doi: 10.1038/nrn2402
de Wit, J. & Ghosh, A. Specification of synaptic connectivity by cell surface interactions. Nat. Rev. Neurosci. 17, 22–35 (2016).
pubmed: 26656254
Polepalli, J. S. et al. Modulation of excitation on parvalbumin interneurons by neuroligin-3 regulates the hippocampal network. Nat. Neurosci. 20, 219–229 (2017).
pubmed: 28067903
pmcid: 5272845
doi: 10.1038/nn.4471
Favuzzi, E. & Rico, B. Molecular diversity underlying cortical excitatory and inhibitory synapse development. Curr. Opin. Neurobiol. 53, 8–15 (2018).
pubmed: 29704699
doi: 10.1016/j.conb.2018.03.011
Favuzzi, E. et al. Distinct molecular programs regulate synapse specificity in cortical inhibitory circuits. Science 363, 413–417 (2019).
pubmed: 30679375
doi: 10.1126/science.aau8977
Fazzari, P. et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464, 1376–1380 (2010).
pubmed: 20393464
doi: 10.1038/nature08928
Exposito-Alonso, D. et al. Subcellular sorting of neuregulins controls the assembly of excitatory-inhibitory cortical circuits. Elife 9, e57000 (2020).
pubmed: 33320083
pmcid: 7755390
doi: 10.7554/eLife.57000
de la Torre-Ubieta, L., Won, H., Stein, J. L. & Geschwind, D. H. Advancing the understanding of autism disease mechanisms through genetics. Nat. Med. 22, 345–361 (2016).
pubmed: 27050589
pmcid: 5072455
doi: 10.1038/nm.4071
Polioudakis, D. et al. A single-cell transcriptomic atlas of human neocortical development during mid-gestation. Neuron 103, 785–801 (2019).
pubmed: 31303374
pmcid: 6831089
doi: 10.1016/j.neuron.2019.06.011
Velmeshev, D. et al. Single-cell genomics identifies cell type-specific molecular changes in autism. Science 364, 685–689 (2019).
pubmed: 31097668
pmcid: 7678724
doi: 10.1126/science.aav8130
Gandal, M. J. et al. Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder. Science 362, eaat8127 (2018).
pubmed: 30545856
pmcid: 6443102
doi: 10.1126/science.aat8127
Helt, M. et al. Can children with autism recover? If so, how? Neuropsychol. Rev. 18, 339–366 (2008).
pubmed: 19009353
doi: 10.1007/s11065-008-9075-9
Shattuck, P. T. et al. Change in autism symptoms and maladaptive behaviors in adolescents and adults with an autism spectrum disorder. J. Autism Dev. Disord. 37, 1735–1747 (2007).
pubmed: 17146700
doi: 10.1007/s10803-006-0307-7
Gouwens, N. W. et al. Integrated morphoelectric and transcriptomic classification of cortical GABAergic cells. Cell 183, 935–953 (2020).
pubmed: 33186530
pmcid: 7781065
doi: 10.1016/j.cell.2020.09.057
Krienen, F. M. et al. Innovations present in the primate interneuron repertoire. Nature 586, 262–269 (2020).
pubmed: 32999462
pmcid: 7957574
doi: 10.1038/s41586-020-2781-z
Tasic, B. et al. Adult mouse cortical cell taxonomy revealed by single-cell transcriptomics. Nat. Neurosci. 19, 335–346 (2016).
pubmed: 26727548
pmcid: 4985242
doi: 10.1038/nn.4216
Lu, H. et al. Loss and gain of MeCP2 cause similar hippocampal circuit dysfunction that is rescued by deep brain stimulation in a Rett syndrome mouse model. Neuron 91, 739–747 (2016).
pubmed: 27499081
pmcid: 5019177
doi: 10.1016/j.neuron.2016.07.018
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
doi: 10.1038/nn.3415
La Fata, G. et al. FMRP regulates multipolar to bipolar transition affecting neuronal migration and cortical circuitry. Nat. Neurosci. 17, 1693–1700 (2014).
pubmed: 25402856
doi: 10.1038/nn.3870
Cheyne, J. E., Zabouri, N., Baddeley, D. & Lohmann, C. Spontaneous activity patterns are altered in the developing visual cortex of the Fmr1 knockout mouse. Front. Neural Circuits 13, 57 (2019).
pubmed: 31616256
pmcid: 6775252
doi: 10.3389/fncir.2019.00057
Zhang, N. et al. Decreased surface expression of the delta subunit of the GABA
pubmed: 28822839
pmcid: 5612918
doi: 10.1016/j.expneurol.2017.08.008
El Idrissi, A. et al. Decreased GABA
pubmed: 15755515
doi: 10.1016/j.neulet.2004.11.087
Tyzio, R. et al. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343, 675–679 (2014).
pubmed: 24503856
doi: 10.1126/science.1247190
He, Q., Nomura, T., Xu, J. & Contractor, A. The developmental switch in GABA polarity is delayed in Fragile X mice. J. Neurosci. 34, 446–450 (2014).
pubmed: 24403144
pmcid: 6608154
doi: 10.1523/JNEUROSCI.4447-13.2014
Contractor, A., Klyachko, V. A. & Portera-Cailliau, C. Altered neuronal and circuit excitability in Fragile X syndrome. Neuron 87, 699–715 (2015).
pubmed: 26291156
pmcid: 4545495
doi: 10.1016/j.neuron.2015.06.017
Zhang, Y. et al. Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1
pubmed: 25383903
doi: 10.1038/nn.3864
Rotschafer, S. & Razak, K. Altered auditory processing in a mouse model of Fragile X syndrome. Brain Res. 1506, 12–24 (2013).
pubmed: 23458504
doi: 10.1016/j.brainres.2013.02.038
Gibson, J. R., Bartley, A. F., Hays, S. A. & Huber, K. M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of Fragile X syndrome. J. Neurophysiol. 100, 2615–2626 (2008).
pubmed: 18784272
pmcid: 2585391
doi: 10.1152/jn.90752.2008
Chen, Q. et al. Dysfunction of cortical GABAergic neurons leads to sensory hyper-reactivity in a Shank3 mouse model of ASD. Nat. Neurosci. 23, 520–532 (2020).
pubmed: 32123378
pmcid: 7131894
doi: 10.1038/s41593-020-0598-6
Wallace, M. L., Burette, A. C., Weinberg, R. J. & Philpot, B. D. Maternal loss of Ube3a produces an excitatory/inhibitory imbalance through neuron-type-specific synaptic defects. Neuron 74, 793–800 (2012).
pubmed: 22681684
pmcid: 3372864
doi: 10.1016/j.neuron.2012.03.036
Robertson, C. E. & Baron-Cohen, S. Sensory perception in autism. Nat. Rev. Neurosci. 18, 671–684 (2017).
pubmed: 28951611
doi: 10.1038/nrn.2017.112
Antoine, M. W., Langberg, T., Schnepel, P. & Feldman, D. E. Increased excitation–inhibition ratio stabilizes synapse and circuit excitability in four autism mouse models. Neuron 101, 648–661 (2019).
pubmed: 30679017
pmcid: 6733271
doi: 10.1016/j.neuron.2018.12.026
Michaelson, S. D. et al. SYNGAP1 heterozygosity disrupts sensory processing by reducing touch-related activity within somatosensory cortex circuits. Nat. Neurosci. 21, 1–13 (2018).
pubmed: 30455457
pmcid: 6309426
doi: 10.1038/s41593-018-0268-0
Rolls, E. T. & Mills, W. P. C. Computations in the deep vs superficial layers of the cerebral cortex. Neurobiol. Learn. Mem. 145, 205–221 (2017).
pubmed: 29042296
doi: 10.1016/j.nlm.2017.10.011
He, C. X. et al. Tactile defensiveness and impaired adaptation of neuronal activity in the Fmr1 knock-out mouse model of autism. J. Neurosci. 37, 6475–6487 (2017).
pubmed: 28607173
pmcid: 5511879
doi: 10.1523/JNEUROSCI.0651-17.2017
Lovelace, J. W. et al. Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X syndrome. Neurobiol. Dis. 89, 126–135 (2016).
pubmed: 26850918
pmcid: 4785038
doi: 10.1016/j.nbd.2016.02.002
Green, S. A. et al. Neurobiology of sensory overresponsivity in youth with autism spectrum disorders. JAMA Psychiatry 72, 778–786 (2015).
pubmed: 26061819
pmcid: 4861140
doi: 10.1001/jamapsychiatry.2015.0737
Lee, S. H. et al. Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488, 379–383 (2012).
pubmed: 22878719
pmcid: 3422431
doi: 10.1038/nature11312
Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139–1152 (2014).
pubmed: 24630718
pmcid: 4041382
doi: 10.1016/j.cell.2014.01.050
Pi, H. J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521–524 (2013).
pubmed: 24097352
pmcid: 4017628
doi: 10.1038/nature12676
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
doi: 10.1038/s41593-018-0231-0
Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203–225 (2012).
pubmed: 22443509
pmcid: 4049541
doi: 10.1146/annurev-neuro-062111-150444
Grice, S. J. et al. Disordered visual processing and oscillatory brain activity in autism and Williams syndrome. Neuroreport 12, 2697–2700 (2001).
pubmed: 11522950
doi: 10.1097/00001756-200108280-00021
Gandal, M. J. et al. Validating gamma oscillations and delayed auditory responses as translational biomarkers of autism. Biol. Psychiatry 68, 1100–1106 (2010).
pubmed: 21130222
pmcid: 5070466
doi: 10.1016/j.biopsych.2010.09.031
Wilkinson, C. L., Levin, A. R., Gabard-Durnam, L. J., Tager-Flusberg, H. & Nelson, C. A. Reduced frontal gamma power at 24 months is associated with better expressive language in toddlers at risk for autism. Autism Res. 12, 1211–1224 (2019).
pubmed: 31119899
pmcid: 7771228
doi: 10.1002/aur.2131
Ethridge, L. E. et al. Neural synchronization deficits linked to cortical hyper-excitability and auditory hypersensitivity in Fragile X syndrome. Mol. Autism 8, 22 (2017).
pubmed: 28596820
pmcid: 5463459
doi: 10.1186/s13229-017-0140-1
Cardin, J. A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009).
pubmed: 19396156
pmcid: 3655711
doi: 10.1038/nature08002
Sohal, V. S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698–702 (2009).
pubmed: 19396159
pmcid: 3969859
doi: 10.1038/nature07991
Veit, J., Hakim, R., Jadi, M. P., Sejnowski, T. J. & Adesnik, H. Cortical gamma band synchronization through somatostatin interneurons. Nat. Neurosci. 20, 951–959 (2017).
pubmed: 28481348
pmcid: 5511041
doi: 10.1038/nn.4562
Guyon, N. et al. Network asynchrony underlying increased broadband gamma power. J. Neurosci. 41, 2944–2963 (2021).
pubmed: 33593859
pmcid: 8018896
doi: 10.1523/JNEUROSCI.2250-20.2021
Lovelace, J. W., Ethell, I. M., Binder, D. K. & Razak, K. A. Translation-relevant EEG phenotypes in a mouse model of Fragile X syndrome. Neurobiol. Dis. 115, 39–48 (2018).
pubmed: 29605426
pmcid: 5969806
doi: 10.1016/j.nbd.2018.03.012
Kissinger, S. T. et al. Visual experience-dependent oscillations and underlying circuit connectivity changes are impaired in Fmr1 KO mice. Cell Rep. 31, 107486 (2020).
pubmed: 32268079
pmcid: 7201849
doi: 10.1016/j.celrep.2020.03.050
Pirbhoy, P. S. et al. Acute pharmacological inhibition of matrix metalloproteinase-9 activity during development restores perineuronal net formation and normalizes auditory processing in Fmr1 KO mice. J. Neurochem. 155, 538–558 (2020).
pubmed: 32374912
pmcid: 7644613
doi: 10.1111/jnc.15037
Radwan, B., Dvorak, D. & Fenton, A. A. Impaired cognitive discrimination and discoordination of coupled theta-gamma oscillations in Fmr1 knockout mice. Neurobiol. Dis. 88, 125–138 (2016).
pubmed: 26792400
pmcid: 4758895
doi: 10.1016/j.nbd.2016.01.003
Talbot, Z. N. et al. Normal CA1 place fields but discoordinated network discharge in a Fmr1-null mouse model of Fragile X syndrome. Neuron 97, 684–697 (2018).
pubmed: 29358017
pmcid: 6066593
doi: 10.1016/j.neuron.2017.12.043
Mukherjee, A., Carvalho, F., Eliez, S. & Caroni, P. Long-lasting rescue of network and cognitive dysfunction in a genetic schizophrenia model. Cell 178, 1387–1402 (2019).
pubmed: 31474363
doi: 10.1016/j.cell.2019.07.023
Cheaha, D. & Kumarnsit, E. Alteration of spontaneous spectral powers and coherences of local field potential in prenatal valproic acid mouse model of autism. Acta Neurobiol. Exp. 75, 351–363 (2015).
Berzhanskaya, J., Phillips, M. A., Shen, J. & Colonnese, M. T. Sensory hypo-excitability in a rat model of fetal development in Fragile X syndrome. Sci. Rep. 6, 30769 (2016).
pubmed: 27465362
pmcid: 4964352
doi: 10.1038/srep30769
Marissal, T. et al. Restoring wild-type-like CA1 network dynamics and behavior during adulthood in a mouse model of schizophrenia. Nat. Neurosci. 21, 1412–1420 (2018).
pubmed: 30224804
pmcid: 6978142
doi: 10.1038/s41593-018-0225-y
Selimbeyoglu, A. et al. Modulation of prefrontal cortex excitation/inhibition balance rescues social behavior in CNTNAP2-deficient mice. Sci. Transl. Med. 9, eaah6733 (2017).
pubmed: 28768803
pmcid: 5723386
doi: 10.1126/scitranslmed.aah6733
Kozono, N., Okamura, A., Honda, S., Matsumoto, M. & Mihara, T. Gamma power abnormalities in a Fmr1-targeted transgenic rat model of Fragile X syndrome. Sci. Rep. 10, 18799 (2020).
pubmed: 33139785
pmcid: 7608556
doi: 10.1038/s41598-020-75893-x
Wohr, M. et al. Lack of parvalbumin in mice leads to behavioral deficits relevant to all human autism core symptoms and related neural morphofunctional abnormalities. Transl. Psychiatry 5, e525 (2015).
pubmed: 25756808
pmcid: 4354349
doi: 10.1038/tp.2015.19
Deng, X., Gu, L., Sui, N., Guo, J. & Liang, J. Parvalbumin interneuron in the ventral hippocampus functions as a discriminator in social memory. Proc. Natl Acad. Sci. USA 116, 16583–16592 (2019).
pubmed: 31358646
pmcid: 6697894
doi: 10.1073/pnas.1819133116
Yizhar, O. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171–178 (2011).
pubmed: 21796121
pmcid: 4155501
doi: 10.1038/nature10360
Andersen, J. et al. Generation of functional human 3D cortico-motor assembloids. Cell 183, 1913–1929 (2020).
pubmed: 33333020
pmcid: 8711252
doi: 10.1016/j.cell.2020.11.017
Kang, Y. et al. A human forebrain organoid model of Fragile X syndrome exhibits altered neurogenesis and highlights new treatment strategies. Nat. Neurosci. 24, 1377–1391 (2021).
pubmed: 34413513
pmcid: 8484073
doi: 10.1038/s41593-021-00913-6
Donegan, J. J., Boley, A. M. & Lodge, D. J. Embryonic stem cell transplants as a therapeutic strategy in a rodent model of autism. Neuropsychopharmacology 43, 1789–1798 (2018).
pubmed: 29453447
pmcid: 6006318
doi: 10.1038/s41386-018-0021-0
Banerjee, A. et al. Jointly reduced inhibition and excitation underlies circuit-wide changes in cortical processing in Rett syndrome. Proc. Natl Acad. Sci. USA 113, E7287–E7296 (2016).
pubmed: 27803317
pmcid: 5135376
doi: 10.1073/pnas.1615330113
Krishnan, K. et al. MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proc. Natl Acad. Sci. USA 112, E4782–E4791 (2015).
pubmed: 26261347
pmcid: 4553776
doi: 10.1073/pnas.1506499112
Lazaro, M. T. et al. Reduced prefrontal synaptic connectivity and disturbed oscillatory population dynamics in the CNTNAP2 model of autism. Cell Rep. 27, 2567–2578 (2019).
pubmed: 31141683
pmcid: 6553483
doi: 10.1016/j.celrep.2019.05.006
Rotaru, D. C., van Woerden, G. M., Wallaard, I. & Elgersma, Y. Adult Ube3a gene reinstatement restores the electrophysiological deficits of prefrontal cortex layer 5 neurons in a mouse model of Angelman syndrome. J. Neurosci. 38, 8011–8030 (2018).
pubmed: 30082419
pmcid: 6596147
doi: 10.1523/JNEUROSCI.0083-18.2018
Mao, W. et al. Shank1 regulates excitatory synaptic transmission in mouse hippocampal parvalbumin-expressing inhibitory interneurons. Eur. J. Neurosci. 41, 1025–1035 (2015).
pubmed: 25816842
pmcid: 4405481
doi: 10.1111/ejn.12877
Berryer, M. H. et al. Decrease of SYNGAP1 in GABAergic cells impairs inhibitory synapse connectivity, synaptic inhibition and cognitive function. Nat. Commun. 7, 13340 (2016).
pubmed: 27827368
pmcid: 5105197
doi: 10.1038/ncomms13340
Codagnone, M. G. et al. Programming bugs: microbiota and the developmental origins of brain health and disease. Biol. Psychiatry 85, 150–163 (2019).
pubmed: 30064690
doi: 10.1016/j.biopsych.2018.06.014
Buffington, S. A. et al. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 165, 1762–1775 (2016).
pubmed: 27315483
pmcid: 5102250
doi: 10.1016/j.cell.2016.06.001
Hsiao, E. Y. et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155, 1451–1463 (2013).
pubmed: 24315484
pmcid: 3897394
doi: 10.1016/j.cell.2013.11.024
Azhari, A., Azizan, F. & Esposito, G. A systematic review of gut-immune-brain mechanisms in Autism Spectrum Disorder. Dev. Psychobiol. 61, 752–771 (2019).
pubmed: 30523646
doi: 10.1002/dev.21803
Han, V. X. et al. Maternal acute and chronic inflammation in pregnancy is associated with common neurodevelopmental disorders: a systematic review. Transl. Psychiatry 11, 71 (2021).
pubmed: 33479207
pmcid: 7820474
doi: 10.1038/s41398-021-01198-w
Shi, L., Fatemi, S. H., Sidwell, R. W. & Patterson, P. H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23, 297–302 (2003).
pubmed: 12514227
pmcid: 6742135
doi: 10.1523/JNEUROSCI.23-01-00297.2003
Shin Yim, Y. et al. Reversing behavioural abnormalities in mice exposed to maternal inflammation. Nature 549, 482–487 (2017).
pubmed: 28902835
doi: 10.1038/nature23909
Vasistha, N. A. et al. Maternal inflammation has a profound effect on cortical interneuron development in a stage and subtype-specific manner. Mol. Psychiatry 25, 2313–2329 (2020).
pubmed: 31595033
doi: 10.1038/s41380-019-0539-5
Donato, F., Rompani, S. B. & Caroni, P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504, 272–276 (2013).
pubmed: 24336286
doi: 10.1038/nature12866
Dehorter, N. et al. Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch. Science 349, 1216–1220 (2015).
pubmed: 26359400
pmcid: 4702376
doi: 10.1126/science.aab3415
Guo, J. & Anton, E. S. Decision making during interneuron migration in the developing cerebral cortex. Trends Cell Biol. 24, 342–351 (2014).
pubmed: 24388877
pmcid: 4299592
doi: 10.1016/j.tcb.2013.12.001
Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M. & Herkenham, M. Maternal immune activation by LPS selectively alters specific gene expression profiles of interneuron migration and oxidative stress in the fetus without triggering a fetal immune response. Brain Behav. Immun. 26, 623–634 (2012).
pubmed: 22310921
pmcid: 3285385
doi: 10.1016/j.bbi.2012.01.015
Su, P. et al. Disruption of SynGAP–dopamine D1 receptor complexes alters actin and microtubule dynamics and impairs GABAergic interneuron migration. Sci. Signal 12, eaau9122 (2019).
pubmed: 31387938
doi: 10.1126/scisignal.aau9122
Ruden, J. B., Dugan, L. L. & Konradi, C. Parvalbumin interneuron vulnerability and brain disorders. Neuropsychopharmacology 46, 279–287 (2021).
pubmed: 32722660
doi: 10.1038/s41386-020-0778-9
Itami, C., Kimura, F. & Nakamura, S. Brain-derived neurotrophic factor regulates the maturation of layer 4 fast-spiking cells after the second postnatal week in the developing barrel cortex. J. Neurosci. 27, 2241–2252 (2007).
pubmed: 17329421
pmcid: 6673466
doi: 10.1523/JNEUROSCI.3345-06.2007
Hampson, D. R., Hooper, A. W. M. & Niibori, Y. The application of adeno-associated viral vector gene therapy to the treatment of Fragile X syndrome. Brain Sci. 9, 32 (2019).
pmcid: 6406794
doi: 10.3390/brainsci9020032
Mossner, J. M., Batista-Brito, R., Pant, R. & Cardin, J. A. Developmental loss of MeCP2 from VIP interneurons impairs cortical function and behavior. Elife 9, e55639 (2020).
pubmed: 32343226
pmcid: 7213975
doi: 10.7554/eLife.55639
Lovelace, J. W. et al. Deletion of Fmr1 from forebrain excitatory neurons triggers abnormal cellular, EEG, and behavioral phenotypes in the auditory cortex of a mouse model of Fragile X syndrome. Cereb. Cortex 30, 969–988 (2020).
pubmed: 31364704
doi: 10.1093/cercor/bhz141