{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T10:14:40Z","timestamp":1790763280950,"version":"4.1.0"},"reference-count":106,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T00:00:00Z","timestamp":1576108800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T00:00:00Z","timestamp":1576108800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T00:00:00Z","timestamp":1576108800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["NS102456"],"award-info":[{"award-number":["NS102456"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000050","name":"National Heart, Lung, and Blood Institute","doi-asserted-by":"publisher","award":["HL127181"],"award-info":[{"award-number":["HL127181"]}],"id":[{"id":"10.13039\/100000050","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Human mutations in the dystroglycan complex (DGC) result in not only muscular dystrophy but also cognitive impairments. However, the molecular architecture critical for the synaptic organization of the DGC in neurons remains elusive. Here, we report Inhibitory Synaptic protein 1 (InSyn1) is a critical component of the DGC whose loss alters the composition of the GABAergic synapses, excitatory\/inhibitory balance in vitro and in vivo, and cognitive behavior. Association of InSyn1 with DGC subunits is required for InSyn1 synaptic localization. InSyn1 null neurons also show a significant reduction in DGC and GABA receptor distribution as well as abnormal neuronal network activity. Moreover, InSyn1 null mice exhibit elevated neuronal firing patterns in the hippocampus and deficits in fear conditioning memory. Our results support the dysregulation of the DGC at inhibitory synapses and altered neuronal network activity and specific cognitive tasks via loss of a novel component, InSyn1.<\/jats:p>","DOI":"10.7554\/elife.50712","type":"journal-article","created":{"date-parts":[[2019,12,12]],"date-time":"2019-12-12T08:00:18Z","timestamp":1576137618000},"source":"Crossref","is-referenced-by-count":28,"title":["Essential role for InSyn1 in dystroglycan complex integrity and cognitive behaviors in mice"],"prefix":"10.7554","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8478-4460","authenticated-orcid":true,"given":"Akiyoshi","family":"Uezu","sequence":"first","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erin","family":"Hisey","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7031-1478","authenticated-orcid":true,"given":"Yoshihiko","family":"Kobayashi","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yudong","family":"Gao","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tyler WA","family":"Bradshaw","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0359-4620","authenticated-orcid":true,"given":"Patrick","family":"Devlin","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramona","family":"Rodriguiz","sequence":"additional","affiliation":[{"name":"Department of Psychiatry and Behavioral Sciences, Duke University Medical School, Durham, United States"},{"name":"Mouse Behavioral and Neuroendocrine Analysis Core Facility, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4837-0337","authenticated-orcid":true,"given":"Purushothama Rao","family":"Tata","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7808-197X","authenticated-orcid":true,"given":"Scott","family":"Soderling","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Duke University Medical School, Durham, United States"},{"name":"Department of Neurobiology, Duke University Medical School, Durham, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2019,12,12]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2018.00132","article-title":"Common ribs of inhibitory synaptic dysfunction in the umbrella of neurodevelopmental disorders","volume":"11","author":"Ali Rodriguez","year":"2018","journal-title":"Frontiers in Molecular Neuroscience"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1111\/j.1600-0854.2006.00519.x","article-title":"Processing and assembly of the dystrophin glycoprotein complex","volume":"8","author":"Allikian","year":"2007","journal-title":"Traffic"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1007\/BF01188497","article-title":"Characterization of GABAergic neurons in hippocampal cell cultures","volume":"23","author":"Benson","year":"1994","journal-title":"Journal of Neurocytology"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"24232","DOI":"10.1074\/jbc.M010418200","article-title":"Dysbindin, a novel coiled-coil-containing protein that interacts with the dystrobrevins in muscle and brain","volume":"276","author":"Benson","year":"2001","journal-title":"Journal of Biological Chemistry"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"6359","DOI":"10.1523\/JNEUROSCI.3029-16.2017","article-title":"Dentate gyrus contributes to retrieval as well as encoding: evidence from context fear conditioning, recall, and extinction","volume":"37","author":"Bernier","year":"2017","journal-title":"The Journal of Neuroscience"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"1263","DOI":"10.1038\/nn1525","article-title":"Millisecond-timescale, genetically targeted optical control of neural activity","volume":"8","author":"Boyden","year":"2005","journal-title":"Nature Neuroscience"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1016\/S0092-8674(00)81053-3","article-title":"Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains","volume":"84","author":"Brenman","year":"1996","journal-title":"Cell"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"4805","DOI":"10.1523\/JNEUROSCI.22-12-04805.2002","article-title":"GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin","volume":"22","author":"Br\u00fcnig","year":"2002","journal-title":"The Journal of Neuroscience"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1016\/S0962-8924(00)01898-5","article-title":"Coiled coils: a highly versatile protein folding motif","volume":"11","author":"Burkhard","year":"2001","journal-title":"Trends in Cell Biology"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"2447","DOI":"10.1523\/JNEUROSCI.4433-10.2011","article-title":"WRP\/srGAP3 facilitates the initiation of spine development by an inverse F-BAR domain, and its loss impairs long-term memory","volume":"31","author":"Carlson","year":"2011","journal-title":"Journal of Neuroscience"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"1174","DOI":"10.1016\/j.jmb.2007.06.019","article-title":"Association of dystrobrevin and regulatory subunit of protein kinase A: a new role for dystrobrevin as a scaffold for signaling proteins","volume":"371","author":"Ceccarini","year":"2007","journal-title":"Journal of Molecular Biology"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.nlm.2015.07.006","article-title":"Cognitive dysfunction in the dystrophin-deficient mouse model of duchenne muscular dystrophy: a reappraisal from sensory to executive processes","volume":"124","author":"Chaussenot","year":"2015","journal-title":"Neurobiology of Learning and Memory"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1038\/nature12354","article-title":"Ultrasensitive fluorescent proteins for imaging neuronal activity","volume":"499","author":"Chen","year":"2013","journal-title":"Nature"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.brainres.2006.03.049","article-title":"Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development","volume":"1093","author":"Chiappalone","year":"2006","journal-title":"Brain Research"},{"key":"bib15","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.brainres.2008.06.022","article-title":"Determinants of spontaneous activity in networks of cultured Hippocampus","volume":"1235","author":"Cohen","year":"2008","journal-title":"Brain Research"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"28387","DOI":"10.1074\/jbc.M402604200","article-title":"The potassium channel Kir4.1 Associates with the Dystrophin-Glycoprotein Complex via \u03b1-Syntrophin in Glia","volume":"279","author":"Connors","year":"2004","journal-title":"Journal of Biological Chemistry"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"4672","DOI":"10.1074\/jbc.M106879200","article-title":"Dystroglycan is not required for localization of dystrophin, Syntrophin, and neuronal nitric-oxide synthase at the sarcolemma but regulates integrin alpha 7B expression and caveolin-3 distribution","volume":"277","author":"C\u00f4t\u00e9","year":"2002","journal-title":"Journal of Biological Chemistry"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1016\/j.nbd.2011.05.012","article-title":"Rescue of a dystrophin-like protein by exon skipping normalizes synaptic plasticity in the Hippocampus of the mdx mouse","volume":"43","author":"Dall\u00e9rac","year":"2011","journal-title":"Neurobiology of Disease"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.neuron.2016.02.019","article-title":"Distinct contribution of Adult-Born hippocampal granule cells to context encoding","volume":"90","author":"Danielson","year":"2016","journal-title":"Neuron"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.celrep.2017.09.025","article-title":"An essential role for the tetraspanin LHFPL4 in the Cell-Type-Specific targeting and clustering of synaptic GABA Receptors","volume":"21","author":"Davenport","year":"2017","journal-title":"Cell Reports"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1038\/ejhg.2013.169","article-title":"A 3-base pair deletion, c.9711_9713del, in DMD results in intellectual disability without muscular dystrophy","volume":"22","author":"de Brouwer","year":"2014","journal-title":"European Journal of Human Genetics"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.neuron.2014.05.018","article-title":"Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis","volume":"83","author":"Denny","year":"2014","journal-title":"Neuron"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1097\/FBP.0b013e3282de7929","article-title":"The role of Hippocampus in anxiety: intracerebral infusion studies","volume":"18","author":"Engin","year":"2007","journal-title":"Behavioural Pharmacology"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1038\/2798","article-title":"Postsynaptic clustering of major GABAA receptor subtypes requires the \u03b32 subunit and gephyrin","volume":"1","author":"Essrich","year":"1998","journal-title":"Nature Neuroscience"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.neuron.2007.09.012","article-title":"Perisomatic inhibition","volume":"56","author":"Freund","year":"2007","journal-title":"Neuron"},{"key":"bib26","doi-asserted-by":"publisher","DOI":"10.3389\/neuro.02.005.2008","article-title":"Epilepsy, E\/I balance and GABA(A) Receptor plasticity","volume":"1","author":"Fritschy","year":"2008","journal-title":"Frontiers in Molecular Neuroscience"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"10296","DOI":"10.1523\/JNEUROSCI.1823-16.2016","article-title":"Neuronal dystroglycan is necessary for formation and maintenance of functional CCK-Positive basket cell terminals on pyramidal cells","volume":"36","author":"Fr\u00fch","year":"2016","journal-title":"The Journal of Neuroscience"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1016\/j.neuron.2019.05.047","article-title":"Plug-and-Play protein modification using Homology-Independent universal genome engineering","volume":"103","author":"Gao","year":"2019","journal-title":"Neuron"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"596","DOI":"10.1016\/j.neuron.2017.12.038","article-title":"Clptm1 limits forward trafficking of GABAA Receptors to Scale Inhibitory Synaptic Strength","volume":"97","author":"Ge","year":"2018","journal-title":"Neuron"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"871","DOI":"10.1038\/nmeth.1694","article-title":"Miniaturized integration of a fluorescence microscope","volume":"8","author":"Ghosh","year":"2011","journal-title":"Nature Methods"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"278","DOI":"10.1016\/j.gde.2011.02.001","article-title":"Dystroglycanopathies: coming into focus","volume":"21","author":"Godfrey","year":"2011","journal-title":"Current Opinion in Genetics & Development"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"2841","DOI":"10.1523\/JNEUROSCI.4823-05.2006","article-title":"Cerebellar synaptic defects and abnormal motor behavior in mice lacking\u00a0- and beta-Dystrobrevin","volume":"26","author":"Grady","year":"2006","journal-title":"Journal of Neuroscience"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1038\/nn.2495","article-title":"Ultrafast optogenetic control","volume":"13","author":"Gunaydin","year":"2010","journal-title":"Nature Neuroscience"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"1056","DOI":"10.1109\/TBME.2006.873392","article-title":"Neural spike train synchronization indices: definitions, interpretations, and applications","volume":"53","author":"Halliday","year":"2006","journal-title":"IEEE Transactions on Biomedical Engineering"},{"key":"bib35","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0039572","article-title":"The biochemical anatomy of cortical inhibitory synapses","volume":"7","author":"Heller","year":"2012","journal-title":"PLOS ONE"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1177\/0883073807309775","article-title":"Neuropsychiatric disorders in males with duchenne muscular dystrophy: frequency rate of attention-deficit hyperactivity disorder (ADHD), autism spectrum disorder, and obsessive--compulsive disorder","volume":"23","author":"Hendriksen","year":"2008","journal-title":"Journal of Child Neurology"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1016\/j.nlm.2008.06.008","article-title":"The hippocampal dentate gyrus is essential for generating contextual memories of fear and drug-induced reward","volume":"90","author":"Hern\u00e1ndez-Rabaza","year":"2008","journal-title":"Neurobiology of Learning and Memory"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"8973","DOI":"10.1074\/jbc.M113.514992","article-title":"Structure of excitatory synapses and GABAA receptor localization at inhibitory synapses are regulated by neuroplastin-65","volume":"289","author":"Herrera-Molina","year":"2014","journal-title":"Journal of Biological Chemistry"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1016\/j.ejmg.2018.03.005","article-title":"15q24.1 BP4-BP1 microdeletion unmasking paternally inherited functional polymorphisms combined with distal 15q24.2q24.3 duplication in a patient with epilepsy, psychomotor delay, overweight, ventricular arrhythmia","volume":"61","author":"Huynh","year":"2018","journal-title":"European Journal of Medical Genetics"},{"key":"bib40","doi-asserted-by":"publisher","DOI":"10.3791\/2270","article-title":"Quantifying synapses: an Immunocytochemistry-based assay to quantify synapse number","volume":"45","author":"Ippolito","year":"2010","journal-title":"Journal of Visualized Experiments"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.neuron.2016.02.040","article-title":"GABAergic Neuron-Specific loss of Ube3a causes angelman Syndrome-Like EEG abnormalities and enhances seizure susceptibility","volume":"90","author":"Judson","year":"2016","journal-title":"Neuron"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"29350","DOI":"10.1074\/jbc.M114.549279","article-title":"A combined transgenic proteomic analysis and regulated trafficking of neuroligin-2","volume":"289","author":"Kang","year":"2014","journal-title":"Journal of Biological Chemistry"},{"key":"bib43","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.02839","article-title":"Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall","volume":"3","author":"Kim","year":"2014","journal-title":"eLife"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1126\/science.1585183","article-title":"Modality-specific retrograde amnesia of fear","volume":"256","author":"Kim","year":"1992","journal-title":"Science"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"4457","DOI":"10.1046\/j.1460-9568.1999.00887.x","article-title":"Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice)","volume":"11","author":"Knuesel","year":"1999","journal-title":"The European Journal of Neuroscience"},{"key":"bib46","doi-asserted-by":"crossref","first-page":"2870","DOI":"10.1016\/S0021-9258(17)42023-0","article-title":"Association of utrophin and multiple dystrophin short forms with the mammalian M(r) 58,000 dystrophin-associated protein (syntrophin)","volume":"269","author":"Kramarcy","year":"1994","journal-title":"The Journal of Biological Chemistry"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"1168","DOI":"10.1016\/S0028-3908(99)00221-X","article-title":"Differential modulatory actions of the volatile convulsant flurothyl and its anesthetic isomer at inhibitory ligand-gated ion channels","volume":"39","author":"Krasowski","year":"2000","journal-title":"Neuropharmacology"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"858","DOI":"10.1093\/nar\/gkn1006","article-title":"Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features","volume":"37","author":"Lassmann","year":"2009","journal-title":"Nucleic Acids Research"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1038\/nature05453","article-title":"Genome-wide atlas of gene expression in the adult mouse brain","volume":"445","author":"Lein","year":"2007","journal-title":"Nature"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"961","DOI":"10.1126\/science.1135801","article-title":"Pattern separation in the dentate gyrus and CA3 of the Hippocampus","volume":"315","author":"Leutgeb","year":"2007","journal-title":"Science"},{"key":"bib51","doi-asserted-by":"publisher","first-page":"4274","DOI":"10.1523\/JNEUROSCI.22-11-04274.2002","article-title":"Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation","volume":"22","author":"L\u00e9vi","year":"2002","journal-title":"The Journal of Neuroscience"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1038\/nature11028","article-title":"Optogenetic stimulation of a hippocampal engram activates fear memory recall","volume":"484","author":"Liu","year":"2012","journal-title":"Nature"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"1295","DOI":"10.1016\/j.cell.2016.07.041","article-title":"Proteomic analysis of unbounded cellular compartments: synaptic clefts","volume":"166","author":"Loh","year":"2016","journal-title":"Cell"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"4847","DOI":"10.1242\/jcs.00805","article-title":"\u00a0-Dystrobrevin interacts directly with kinesin heavy chain in brain","volume":"116","author":"Macioce","year":"2003","journal-title":"Journal of Cell Science"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.neuron.2004.12.016","article-title":"Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat Hippocampus in vitro","volume":"45","author":"Mann","year":"2005","journal-title":"Neuron"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"897","DOI":"10.1146\/annurev.neuro.24.1.897","article-title":"Neurobiology of pavlovian fear conditioning","volume":"24","author":"Maren","year":"2001","journal-title":"Annual Review of Neuroscience"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/nrn3492","article-title":"The contextual brain: implications for fear conditioning, extinction and psychopathology","volume":"14","author":"Maren","year":"2013","journal-title":"Nature Reviews Neuroscience"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1038\/nrn3155","article-title":"Interneuron dysfunction in psychiatric disorders","volume":"13","author":"Mar\u00edn","year":"2012","journal-title":"Nature Reviews Neuroscience"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/S0006-8993(97)01266-3","article-title":"Production of the fos protein after contextual fear conditioning of C57BL\/6N mice","volume":"784","author":"Milanovic","year":"1998","journal-title":"Brain Research"},{"key":"bib60","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1080\/10799890600920035","article-title":"GABAA receptors in central nervous system disease: anxiety, epilepsy, and insomnia","volume":"26","author":"M\u00f6hler","year":"2006","journal-title":"Journal of Receptor and Signal Transduction Research"},{"key":"bib61","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.30510","article-title":"Automated cell-type classification in intact tissues by single-cell molecular profiling","volume":"7","author":"Nagendran","year":"2018","journal-title":"eLife"},{"key":"bib62","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1016\/j.neuron.2012.10.012","article-title":"Molecular motor KIF5A is essential for GABA(A) receptor transport, and KIF5A deletion causes epilepsy","volume":"76","author":"Nakajima","year":"2012","journal-title":"Neuron"},{"key":"bib63","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M116.724443","article-title":"Proteomic characterization of inhibitory synapses using a novel pHluorin-tagged GABAAR \u03b12 subunit knock-in mouse","author":"Nakamura","year":"2016","journal-title":"Journal of Biological Chemistry"},{"key":"bib64","first-page":"557","article-title":"Nervous system involvement in progressive muscular dystrophy","volume":"5","author":"Nakao","year":"1968","journal-title":"Proceedings of the Australian Association of Neurologists"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"14108","DOI":"10.1073\/pnas.241508198","article-title":"Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein","volume":"98","author":"Neely","year":"2001","journal-title":"PNAS"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"718","DOI":"10.1016\/j.neuron.2018.03.046","article-title":"The GABAA Receptor \u03b2 Subunit Is Required for Inhibitory Transmission","volume":"98","author":"Nguyen","year":"2018","journal-title":"Neuron"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1006\/mgme.2001.3220","article-title":"Dystrophin and muscular dystrophy: past, present, and future","volume":"74","author":"O'Brien","year":"2001","journal-title":"Molecular Genetics and Metabolism"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1124\/pr.108.00505","article-title":"International union of pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. update","volume":"60","author":"Olsen","year":"2008","journal-title":"Pharmacological Reviews"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1038\/nn.3950","article-title":"Microcircuits and their interactions in epilepsy: is the focus out of focus?","volume":"18","author":"Paz","year":"2015","journal-title":"Nature Neuroscience"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"1619","DOI":"10.1152\/physrev.00007.2017","article-title":"Hippocampal GABAergic inhibitory interneurons","volume":"97","author":"Pelkey","year":"2017","journal-title":"Physiological Reviews"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1016\/j.neuron.2013.09.046","article-title":"Theta-gamma-modulated synaptic currents in hippocampal granule cells in vivo define a mechanism for network oscillations","volume":"81","author":"Pern\u00eda-Andrade","year":"2014","journal-title":"Neuron"},{"key":"bib72","doi-asserted-by":"publisher","DOI":"10.1186\/s13395-016-0095-5","article-title":"Characterization of a dmd (EGFP) reporter mouse as a tool to investigate dystrophin expression","volume":"6","author":"Petkova","year":"2016","journal-title":"Skeletal Muscle"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1037\/0735-7044.106.2.274","article-title":"Differential contribution of amygdala and Hippocampus to cued and contextual fear conditioning","volume":"106","author":"Phillips","year":"1992","journal-title":"Behavioral Neuroscience"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"6590","DOI":"10.1523\/JNEUROSCI.0753-07.2007","article-title":"Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures","volume":"27","author":"Polack","year":"2007","journal-title":"Journal of Neuroscience"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1111\/j.1601-183X.2009.00555.x","article-title":"Mice lacking synapsin III show abnormalities in explicit memory and conditioned fear","volume":"9","author":"Porton","year":"2010","journal-title":"Genes, Brain and Behavior"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"6810","DOI":"10.1073\/pnas.1321774111","article-title":"Dystroglycan mediates homeostatic synaptic plasticity at GABAergic synapses","volume":"111","author":"Pribiag","year":"2014","journal-title":"PNAS"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"582","DOI":"10.1038\/338582a0","article-title":"Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology","volume":"338","author":"Pritchett","year":"1989","journal-title":"Nature"},{"key":"bib78","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1126\/science.1239073","article-title":"Creating a false memory in the Hippocampus","volume":"341","author":"Ramirez","year":"2013","journal-title":"Science"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"1230","DOI":"10.1126\/science.1143839","article-title":"Localization of a stable neural correlate of associative memory","volume":"317","author":"Reijmers","year":"2007","journal-title":"Science"},{"key":"bib80","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1016\/j.neuron.2009.06.016","article-title":"Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation","volume":"63","author":"Roberts","year":"2009","journal-title":"Neuron"},{"key":"bib81","volume-title":"Animal Models of Cognitive Impairment","author":"Rodriguiz","year":"2006"},{"key":"bib82","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1126\/science.aaa5542","article-title":"Engram cells retain memory under retrograde amnesia","volume":"348","author":"Ryan","year":"2015","journal-title":"Science"},{"key":"bib83","doi-asserted-by":"publisher","first-page":"12413","DOI":"10.1073\/pnas.94.23.12413","article-title":"Dystrobrevin and dystrophin: an interaction through coiled-coil motifs","volume":"94","author":"Sadoulet-Puccio","year":"1997","journal-title":"PNAS"},{"key":"bib84","doi-asserted-by":"publisher","first-page":"14201","DOI":"10.1074\/jbc.M111.293175","article-title":"The cell adhesion molecule Neuroplastin-65 is a novel interaction partner of \u03b3-Aminobutyric acid type A receptors","volume":"287","author":"Sarto-Jackson","year":"2012","journal-title":"Journal of Biological Chemistry"},{"key":"bib85","doi-asserted-by":"publisher","first-page":"3056","DOI":"10.1523\/JNEUROSCI.5422-05.2006","article-title":"Impaired feedforward inhibition of the thalamocortical projection in epileptic Ca2+ channel mutant mice, tottering","volume":"26","author":"Sasaki","year":"2006","journal-title":"Journal of Neuroscience"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1083\/jcb.200105003","article-title":"A stoichiometric complex of neurexins and dystroglycan in brain","volume":"154","author":"Sugita","year":"2001","journal-title":"The Journal of Cell Biology"},{"key":"bib87","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1111\/j.1471-4159.2006.04170.x","article-title":"Synaptic scaffolding molecule (S-SCAM) membrane-associated guanylate kinase with inverted organization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons","volume":"100","author":"Sumita","year":"2007","journal-title":"Journal of Neurochemistry"},{"key":"bib88","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1097\/00019052-199510000-00010","article-title":"Dystrophin-glycoprotein complex: molecular organization and critical roles in skeletal muscle","volume":"8","author":"Sunada","year":"1995","journal-title":"Current Opinion in Neurology"},{"key":"bib89","doi-asserted-by":"publisher","first-page":"3073","DOI":"10.1152\/jn.00995.2015","article-title":"Network burst activity in hippocampal neuronal cultures: the role of synaptic and intrinsic currents","volume":"115","author":"Suresh","year":"2016","journal-title":"Journal of Neurophysiology"},{"key":"bib90","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1038\/nature20565","article-title":"In vivo genome editing via CRISPR\/Cas9 mediated homology-independent targeted integration","volume":"540","author":"Suzuki","year":"2016","journal-title":"Nature"},{"key":"bib91","doi-asserted-by":"publisher","first-page":"17536","DOI":"10.1073\/pnas.0708440104","article-title":"Reduced cortical inhibition in a mouse model of familial childhood absence epilepsy","volume":"104","author":"Tan","year":"2007","journal-title":"PNAS"},{"key":"bib92","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-00333-w","article-title":"IgSF21 promotes differentiation of inhibitory synapses via binding to neurexin2\u03b1","volume":"8","author":"Tanabe","year":"2017","journal-title":"Nature Communications"},{"key":"bib93","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1242\/jcs.158337","article-title":"Selective synaptic targeting of the excitatory and inhibitory presynaptic organizers FGF22 and FGF7","volume":"128","author":"Terauchi","year":"2015","journal-title":"Journal of Cell Science"},{"key":"bib94","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.neuron.2009.12.007","article-title":"Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin","volume":"65","author":"Twelvetrees","year":"2010","journal-title":"Neuron"},{"key":"bib95","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1038\/nrn3670","article-title":"Gephyrin: a master regulator of neuronal function?","volume":"15","author":"Tyagarajan","year":"2014","journal-title":"Nature Reviews Neuroscience"},{"key":"bib96","doi-asserted-by":"publisher","first-page":"E2929","DOI":"10.1073\/pnas.1207358109","article-title":"Modified SH2 domain to phototrap and identify phosphotyrosine proteins from subcellular sites within cells","volume":"109","author":"Uezu","year":"2012","journal-title":"PNAS"},{"key":"bib97","doi-asserted-by":"publisher","first-page":"1123","DOI":"10.1126\/science.aag0821","article-title":"Identification of an elaborate complex mediating postsynaptic inhibition","volume":"353","author":"Uezu","year":"2016","journal-title":"Science"},{"key":"bib98","doi-asserted-by":"publisher","first-page":"1683","DOI":"10.1038\/mt.2010.134","article-title":"Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAA-receptor clustering in the Hippocampus of the mdx mouse","volume":"18","author":"Vaillend","year":"2010","journal-title":"Molecular Therapy"},{"key":"bib99","doi-asserted-by":"publisher","first-page":"1041","DOI":"10.1093\/hmg\/ddx013","article-title":"Relationships linking emotional, motor, cognitive and GABAergic dysfunctions in dystrophin-deficient mdx mice","volume":"26","author":"Vaillend","year":"2017","journal-title":"Human Molecular Genetics"},{"key":"bib100","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1038\/nmeth.3365","article-title":"High-performance probes for light and electron microscopy","volume":"12","author":"Viswanathan","year":"2015","journal-title":"Nature Methods"},{"key":"bib101","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1016\/j.tins.2012.04.004","article-title":"The dystrophin-glycoprotein complex in brain development and disease","volume":"35","author":"Waite","year":"2012","journal-title":"Trends in Neurosciences"},{"key":"bib102","doi-asserted-by":"publisher","first-page":"961","DOI":"10.1016\/j.cell.2016.09.051","article-title":"Distinct hippocampal pathways mediate dissociable roles of context in memory retrieval","volume":"167","author":"Xu","year":"2016","journal-title":"Cell"},{"key":"bib103","doi-asserted-by":"publisher","first-page":"1138","DOI":"10.1016\/j.neuron.2017.02.023","article-title":"GARLH family proteins stabilize GABAA Receptors at Synapses","volume":"93","author":"Yamasaki","year":"2017","journal-title":"Neuron"},{"key":"bib104","doi-asserted-by":"publisher","first-page":"4975","DOI":"10.1074\/jbc.270.10.4975","article-title":"Identification of alpha-syntrophin binding to syntrophin triplet, dystrophin, and utrophin","volume":"270","author":"Yang","year":"1995","journal-title":"Journal of Biological Chemistry"},{"key":"bib105","doi-asserted-by":"publisher","first-page":"8462","DOI":"10.1523\/JNEUROSCI.3624-13.2014","article-title":"Neuronal ensembles in Amygdala, Hippocampus, and prefrontal cortex track differential components of contextual fear","volume":"34","author":"Zelikowsky","year":"2014","journal-title":"Journal of Neuroscience"},{"key":"bib106","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a009886","article-title":"Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities","volume":"4","author":"Zoghbi","year":"2012","journal-title":"Cold Spring Harbor Perspectives in Biology"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/50712\/elife-50712-v2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/50712\/elife-50712-v2.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/50712","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T21:04:05Z","timestamp":1697058245000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/50712"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,12]]},"references-count":106,"alternative-id":["10.7554\/eLife.50712"],"URL":"https:\/\/doi.org\/10.7554\/elife.50712","archive":["CLOCKSS"],"relation":{"has-review":[{"id-type":"doi","id":"10.7554\/eLife.50712.sa1","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.50712.sa2","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,12]]},"article-number":"e50712"}}