{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,25]],"date-time":"2026-08-25T23:55:45Z","timestamp":1787702145652,"version":"build-2784847793"},"reference-count":138,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2024,2,2]],"date-time":"2024-02-02T00:00:00Z","timestamp":1706832000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32170828"],"award-info":[{"award-number":["32170828"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2021YFA0909300"],"award-info":[{"award-number":["2021YFA0909300"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Ministry of Science and Technology, China","award":["32170828"],"award-info":[{"award-number":["32170828"]}]},{"name":"Ministry of Science and Technology, China","award":["2021YFA0909300"],"award-info":[{"award-number":["2021YFA0909300"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Sciences"],"abstract":"<jats:p>Chemical synapses are essential for neuronal information storage and relay. The synaptic signal received or sent from spatially distinct subcellular compartments often generates different outcomes due to the distance or physical property difference. Therefore, the final output of postsynaptic neurons is determined not only by the type and intensity of synaptic inputs but also by the synaptic subcellular location. How synaptic subcellular specificity is determined has long been the focus of study in the neurodevelopment field. Genetic studies from invertebrates such as Caenorhabditis elegans (C. elegans) have uncovered important molecular and cellular mechanisms required for subcellular specificity. Interestingly, similar molecular mechanisms were found in the mammalian cerebellum, hippocampus, and cerebral cortex. This review summarizes the comprehensive advances in the cellular and molecular mechanisms underlying synaptic subcellular specificity, focusing on studies from C. elegans and rodents.<\/jats:p>","DOI":"10.3390\/brainsci14020155","type":"journal-article","created":{"date-parts":[[2024,2,2]],"date-time":"2024-02-02T09:24:08Z","timestamp":1706865848000},"page":"155","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Cellular and Molecular Mechanisms Underlying Synaptic Subcellular Specificity"],"prefix":"10.3390","volume":"14","author":[{"given":"Mengqing","family":"Wang","sequence":"first","affiliation":[{"name":"State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Institutes of Brain Science, Department of Neurosurgery, Zhongshan Hospital, Fudan University, 131 Dong An Rd, Research Building B4017, Shanghai 200032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiale","family":"Fan","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Institutes of Brain Science, Department of Neurosurgery, Zhongshan Hospital, Fudan University, 131 Dong An Rd, Research Building B4017, Shanghai 200032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6475-7681","authenticated-orcid":false,"given":"Zhiyong","family":"Shao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Institutes of Brain Science, Department of Neurosurgery, Zhongshan Hospital, Fudan University, 131 Dong An Rd, Research Building B4017, Shanghai 200032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,2,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2719","DOI":"10.1007\/s00018-019-03109-1","article-title":"Intrinsic and extrinsic mechanisms of synapse formation and specificity in C. elegans","volume":"76","author":"Hendi","year":"2019","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1007\/s10158-018-0207-5","article-title":"The presynaptic machinery at the synapse of C. elegans","volume":"18","author":"Calahorro","year":"2018","journal-title":"Invertebr. Neurosci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1111\/j.1600-0854.2007.00595.x","article-title":"Clathrin-mediated endocytosis at synapses","volume":"8","author":"Jung","year":"2007","journal-title":"Traffic"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/375645a0","article-title":"The synaptic vesicle cycle: A cascade of protein-protein interactions","volume":"375","author":"Sudhof","year":"1995","journal-title":"Nature"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1146\/annurev.neuro.26.041002.131412","article-title":"The synaptic vesicle cycle","volume":"27","author":"Sudhof","year":"2004","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1038\/nrn2699","article-title":"Experience-dependent structural synaptic plasticity in the mammalian brain","volume":"10","author":"Holtmaat","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1016\/j.conb.2013.07.004","article-title":"The cell biology of synaptic specificity during development","volume":"23","author":"Christensen","year":"2013","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1038\/nn1638","article-title":"Subcellular organization of GABAergic synapses: Role of ankyrins and L1 cell adhesion molecules","volume":"9","author":"Huang","year":"2006","journal-title":"Nat. Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1146\/annurev.cellbio.24.110707.175402","article-title":"Many Paths to Synaptic Specificity","volume":"25","author":"Sanes","year":"2009","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1146\/annurev.neuro.051508.135302","article-title":"Genetics and Cell Biology of Building Specific Synaptic Connectivity","volume":"33","author":"Shen","year":"2010","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1146\/annurev-cellbio-100913-012953","article-title":"Cellular and molecular mechanisms of synaptic specificity","volume":"30","author":"Yogev","year":"2014","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1007\/BF01176183","article-title":"The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. I. General description","volume":"5","author":"Peters","year":"1976","journal-title":"J. Neurocytol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2315","DOI":"10.1016\/j.cub.2023.04.071","article-title":"Neuronal contact predicts connectivity in the C. elegans brain","volume":"33","author":"Cook","year":"2023","journal-title":"Curr. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.tins.2016.11.007","article-title":"Weighing the Evidence in Peters\u2019 Rule: Does Neuronal Morphology Predict Connectivity?","volume":"40","author":"Rees","year":"2017","journal-title":"Trends Neurosci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s12565-023-00743-5","article-title":"Synaptic configuration and reconfiguration in the neocortex are spatiotemporally selective","volume":"99","author":"Sohn","year":"2024","journal-title":"Anat. Sci. Int."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1959","DOI":"10.1126\/science.1072165","article-title":"Molecular mechanisms of axon guidance","volume":"298","author":"Dickson","year":"2002","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Kolodkin, A.L., and Tessier-Lavigne, M. (2011). Mechanisms and molecules of neuronal wiring: A primer. Cold Spring Harb. Perspect. Biol., 3.","DOI":"10.1101\/cshperspect.a001727"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1016\/j.gde.2007.05.007","article-title":"Migration of neuronal cells along the anterior-posterior body axis of C. elegans: Wnts are in control","volume":"17","author":"Silhankova","year":"2007","journal-title":"Curr. Opin. Genet. Dev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"dev151415","DOI":"10.1242\/dev.151415","article-title":"Understanding axon guidance: Are we nearly there yet?","volume":"145","author":"Stoeckli","year":"2018","journal-title":"Development"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1126\/science.1143762","article-title":"Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans","volume":"318","author":"Margeta","year":"2007","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"704","DOI":"10.1016\/j.cell.2007.06.046","article-title":"Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans","volume":"130","author":"Klassen","year":"2007","journal-title":"Cell"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.neuron.2012.12.031","article-title":"Interaxonal interaction defines tiled presynaptic innervation in C. elegans","volume":"77","author":"Mizumoto","year":"2013","journal-title":"Neuron"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e43478","DOI":"10.7554\/eLife.43478","article-title":"Regulation of subcellular dendritic synapse specificity by axon guidance cues","volume":"8","author":"Sales","year":"2019","journal-title":"eLife"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"109828","DOI":"10.1016\/j.celrep.2021.109828","article-title":"Synaptogenic activity of the axon guidance molecule Robo2 underlies hippocampal circuit function","volume":"37","author":"Blockus","year":"2021","journal-title":"Cell Rep."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1038\/nature08628","article-title":"Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS","volume":"462","author":"Tran","year":"2009","journal-title":"Nature"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/0896-6273(90)90444-K","article-title":"The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans","volume":"4","author":"Hedgecock","year":"1990","journal-title":"Neuron"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0092-8674(00)81336-7","article-title":"Deleted in Colorectal Cancer (DCC) encodes a netrin receptor","volume":"87","author":"Masu","year":"1996","journal-title":"Cell"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/0092-8674(94)90421-9","article-title":"Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord","volume":"78","author":"Kennedy","year":"1994","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1038\/386833a0","article-title":"Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors","volume":"386","author":"Leonardo","year":"1997","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/S0896-6273(00)80153-1","article-title":"Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons","volume":"17","author":"Mitchell","year":"1996","journal-title":"Neuron"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/S0092-8674(00)81795-X","article-title":"Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system","volume":"87","author":"Serafini","year":"1996","journal-title":"Cell"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/0092-8674(94)90420-0","article-title":"The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6","volume":"78","author":"Serafini","year":"1994","journal-title":"Cell"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1038\/s41380-019-0561-7","article-title":"The Netrin-1\/DCC guidance system: Dopamine pathway maturation and psychiatric disorders emerging in adolescence","volume":"25","author":"Vosberg","year":"2020","journal-title":"Mol. Psychiatry"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S0896-6273(00)80021-5","article-title":"Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans","volume":"16","author":"Wadsworth","year":"1996","journal-title":"Neuron"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"11065","DOI":"10.1523\/JNEUROSCI.0947-09.2009","article-title":"Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain","volume":"29","author":"Manitt","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1523\/JNEUROSCI.3471-12.2012","article-title":"Serotonergic neurosecretory synapse targeting is controlled by netrin-releasing guidepost neurons in Caenorhabditis elegans","volume":"33","author":"Nelson","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1038\/nature07291","article-title":"UNC-6\/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites","volume":"455","author":"Poon","year":"2008","journal-title":"Nature"},{"key":"ref_38","first-page":"1","article-title":"The structure of the nervous system of the nematode Caenorhabditis elegans","volume":"314","author":"White","year":"1986","journal-title":"Philos. Trans. R. Soc. Lond."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"17278","DOI":"10.1523\/JNEUROSCI.1085-13.2013","article-title":"Netrin-1 promotes excitatory synaptogenesis between cortical neurons by initiating synapse assembly","volume":"33","author":"Goldman","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e83760","DOI":"10.7554\/eLife.83760","article-title":"Netrin-1 regulates the balance of synaptic glutamate signaling in the adult ventral tegmental area","volume":"12","author":"Cline","year":"2023","journal-title":"eLife"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/S0092-8674(00)80766-7","article-title":"Unified nomenclature for the semaphorins\/collapsins. Semaphorin Nomenclature Committee","volume":"97","author":"Goodman","year":"1999","journal-title":"Cell"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.conb.2020.12.014","article-title":"Semaphorins and Plexins in central nervous system patterning: The key to it all?","volume":"66","author":"Limoni","year":"2021","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_43","first-page":"327","article-title":"The structure of the ventral nerve cord of Caenorhabditis elegans","volume":"275","author":"White","year":"1976","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e38801","DOI":"10.7554\/eLife.38801","article-title":"Rap2 and TNIK control Plexin-dependent tiled synaptic innervation in C. elegans","volume":"7","author":"Chen","year":"2018","journal-title":"eLife"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1038\/nature09675","article-title":"Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina","volume":"470","author":"Matsuoka","year":"2011","journal-title":"Nature"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Adel, S.S., Pranske, Z.J., Kowalski, T.F., Kanzler, N., Ray, R., Carmona, C., and Paradis, S. (2023). Plexin-B1 and Plexin-B2 play non-redundant roles in GABAergic synapse formation. bioRxiv.","DOI":"10.1101\/2023.10.27.564428"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e04390","DOI":"10.7554\/eLife.04390","article-title":"Semaphorin 5A inhibits synaptogenesis in early postnatal- and adult-born hippocampal dentate granule cells","volume":"3","author":"Duan","year":"2014","journal-title":"eLife"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"8961","DOI":"10.1523\/JNEUROSCI.0989-13.2013","article-title":"The class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus","volume":"33","author":"Kuzirian","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.mcn.2018.06.008","article-title":"Class 4 Semaphorins and Plexin-B receptors regulate GABAergic and glutamatergic synapse development in the mammalian hippocampus","volume":"92","author":"McDermott","year":"2018","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1038\/nrn1665","article-title":"WNTs in the vertebrate nervous system: From patterning to neuronal connectivity","volume":"6","author":"Ciani","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/bs.pmbts.2018.04.005","article-title":"Wnt Signaling in the Hippocampus in Relation to Neurogenesis, Neuroplasticity, Stress and Epigenetics","volume":"158","author":"Zwamborn","year":"2018","journal-title":"Prog. Mol. Biol. Transl. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Anand, A.A., Khan, M., V, M., and Kar, D. (2023). The Molecular Basis of Wnt\/\u03b2-Catenin Signaling Pathways in Neurodegenerative Diseases. Int. J. Cell Biol., 2023.","DOI":"10.1155\/2023\/9296092"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"162","DOI":"10.3389\/fncel.2013.00162","article-title":"Wnts in action: From synapse formation to synaptic maintenance","volume":"7","author":"Dickins","year":"2013","journal-title":"Front. Cell. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"107495","DOI":"10.1016\/j.celrep.2020.03.059","article-title":"Enhancing WNT Signaling Restores Cortical Neuronal Spine Maturation and Synaptogenesis in Tbr1 Mutants","volume":"31","author":"Pai","year":"2020","journal-title":"Cell Rep."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.celrep.2013.09.011","article-title":"Two Wnts instruct topographic synaptic innervation in C. elegans","volume":"5","author":"Mizumoto","year":"2013","journal-title":"Cell Rep."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1186\/1749-8104-3-32","article-title":"Wnts acting through canonical and noncanonical signaling pathways exert opposite effects on hippocampal synapse formation","volume":"3","author":"Davis","year":"2008","journal-title":"Neural Dev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1038\/emboj.2012.145","article-title":"WNTs in synapse formation and neuronal circuitry","volume":"31","author":"Park","year":"2012","journal-title":"EMBO J."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"194","DOI":"10.3389\/fnmol.2018.00194","article-title":"Wnts Promote Synaptic Assembly Through T-Cell Specific Transcription Factors in Caenorhabditis elegans","volume":"11","author":"Shi","year":"2018","journal-title":"Front. Mol. Neurosci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/S0092-8674(00)80689-3","article-title":"Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling","volume":"100","author":"Hall","year":"2000","journal-title":"Cell"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1006\/dbio.1997.8734","article-title":"WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons","volume":"192","author":"Lucas","year":"1997","journal-title":"Dev. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"10732","DOI":"10.1073\/pnas.1018132108","article-title":"Wnt7a signaling promotes dendritic spine growth and synaptic strength through Ca2+\/Calmodulin-dependent protein kinase II","volume":"108","author":"Ciani","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"15857","DOI":"10.1074\/jbc.M808986200","article-title":"Wnt-5a\/JNK signaling promotes the clustering of PSD-95 in hippocampal neurons","volume":"284","author":"Farias","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1111\/jnc.15448","article-title":"Wnt5a modulates dendritic spine dynamics through the regulation of Cofilin via small Rho GTPase activity in hippocampal neurons","volume":"158","author":"Vallejo","year":"2021","journal-title":"J. Neurochem."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e80555","DOI":"10.7554\/eLife.80555","article-title":"Channel-independent function of UNC-9\/Innexin in spatial arrangement of GABAergic synapses in C. elegans","volume":"11","author":"Hendi","year":"2022","journal-title":"eLife"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/S0092-8674(00)80590-5","article-title":"Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance","volume":"96","author":"Brose","year":"1999","journal-title":"Cell"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1016\/S0092-8674(00)80589-9","article-title":"Slit Is the Midline Repellent for the Robo Receptor in Drosophila","volume":"96","author":"Kidd","year":"1999","journal-title":"Cell"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0092-8674(00)80915-0","article-title":"Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors","volume":"92","author":"Kidd","year":"1998","journal-title":"Cell"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3037","DOI":"10.1242\/dev.132829","article-title":"Slit-Robo signaling","volume":"143","author":"Blockus","year":"2016","journal-title":"Development"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1016\/j.ydbio.2019.07.017","article-title":"Slit\/Robo signals prevent spinal motor neuron emigration by organizing the spinal cord basement membrane","volume":"455","author":"Kim","year":"2019","journal-title":"Dev. Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"337","DOI":"10.4161\/cam.4.3.11219","article-title":"Longitudinal axons are guided by Slit\/Robo signals from the floor plate","volume":"4","author":"Mastick","year":"2010","journal-title":"Cell Adhes. Migr."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"592733","DOI":"10.3389\/fonc.2020.592733","article-title":"Cadherins, Selectins, and Integrins in CAM-DR in Leukemia","volume":"10","author":"Kim","year":"2020","journal-title":"Front. Oncol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1038\/s41467-023-36042-w","article-title":"Concerted roles of LRRTM1 and SynCAM 1 in organizing prefrontal cortex synapses and cognitive functions","volume":"14","author":"Ribic","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"112170","DOI":"10.1016\/j.celrep.2023.112170","article-title":"Developmental neuronal origin regulates neocortical map formation","volume":"42","author":"Lin","year":"2023","journal-title":"Cell Rep."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Sudhof, T.C. (2021). The cell biology of synapse formation. J. Cell Biol., 220.","DOI":"10.1083\/jcb.202103052"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1038\/nrn2075","article-title":"Cell adhesion molecules: Signalling functions at the synapse","volume":"8","author":"Dalva","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Galindo, S.E., Shin, G.J., Millard, S.S., and Grueber, W.B. (2023). Regulated alternative splicing of Dscam2 is required for somatosensory circuit wiring. bioRxiv.","DOI":"10.1101\/2023.03.01.530539"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2400","DOI":"10.2741\/1978","article-title":"Cell adhesion molecules at the synapse","volume":"11","author":"Gerrow","year":"2006","journal-title":"Front. Biosci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1002\/(SICI)1097-4547(19991001)58:1<130::AID-JNR13>3.0.CO;2-8","article-title":"Cadherins and synaptic specificity","volume":"58","author":"Redies","year":"1999","journal-title":"J. Neurosci. Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2080","DOI":"10.1016\/j.devcel.2023.07.011","article-title":"Rejection of inappropriate synaptic partners in mouse retina mediated by transcellular FLRT2-UNC5 signaling","volume":"58","author":"Prigge","year":"2023","journal-title":"Dev. Cell"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.tins.2017.03.003","article-title":"Neural Cell Adhesion Molecules of the Immunoglobulin Superfamily Regulate Synapse Formation, Maintenance, and Function","volume":"40","author":"Sytnyk","year":"2017","journal-title":"Trends Neurosci."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"3998","DOI":"10.1016\/j.cub.2023.08.020","article-title":"Brain wiring determinants uncovered by integrating connectomes and transcriptomes","volume":"33","author":"Yoo","year":"2023","journal-title":"Curr. Biol."},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Lee, I.H., Walker, D.I., Lin, Y., Smith, M.R., Mandl, K.D., Jones, D.P., and Kong, S.W. (2023). Association between Neuroligin-1 polymorphism and plasma glutamine levels in individuals with autism spectrum disorder. eBioMedicine, 95.","DOI":"10.1016\/j.ebiom.2023.104746"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Zhang, L., and Wei, X. (2023). SynCAMs in Normal Vertebrate Neural Development and Neuropsychiatric Disorders: From the Perspective of the OCAs. Mol. Neurobiol.","DOI":"10.1007\/s12035-023-03579-2"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1525","DOI":"10.1126\/science.1072356","article-title":"SynCAM, a synaptic adhesion molecule that drives synapse assembly","volume":"297","author":"Biederer","year":"2002","journal-title":"Science"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1016\/S0092-8674(02)00910-8","article-title":"Sidekicks: Synaptic Adhesion Molecules that Promote Lamina-Specific Connectivity in the Retina","volume":"110","author":"Yamagata","year":"2002","journal-title":"Cell"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/S0092-8674(03)00113-2","article-title":"The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans","volume":"112","author":"Shen","year":"2003","journal-title":"Cell"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1016\/S0092-8674(04)00251-X","article-title":"Synaptic Specificity Is Generated by the Synaptic Guidepost Protein SYG-2 and Its Receptor, SYG-1","volume":"116","author":"Shen","year":"2004","journal-title":"Cell"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1038\/nn.2991","article-title":"NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins","volume":"15","author":"Chia","year":"2012","journal-title":"Nat. Neurosci."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.cell.2004.10.004","article-title":"Ankyrin-Based Subcellular Gradient of Neurofascin, an Immunoglobulin Family Protein, Directs GABAergic Innervation at Purkinje Axon Initial Segment","volume":"119","author":"Ango","year":"2004","journal-title":"Cell"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1276","DOI":"10.1016\/j.neuron.2016.08.015","article-title":"Dual Function of NRP1 in Axon Guidance and Subcellular Target Recognition in Cerebellum","volume":"91","author":"Telley","year":"2016","journal-title":"Neuron"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.neuron.2019.02.009","article-title":"Axo-axonic Innervation of Neocortical Pyramidal Neurons by GABAergic Chandelier Cells Requires AnkyrinG-Associated L1CAM","volume":"102","author":"Tai","year":"2019","journal-title":"Neuron"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"2684","DOI":"10.1093\/cercor\/bhq016","article-title":"Perisomatic GABAergic innervation in prefrontal cortex is regulated by ankyrin interaction with the L1 cell adhesion molecule","volume":"20","author":"Guan","year":"2010","journal-title":"Cereb. Cortex"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.neuron.2013.10.060","article-title":"Neuronal Ig\/Caspr Recognition Promotes the Formation of Axoaxonic Synapses in Mouse Spinal Cord","volume":"81","author":"Ashrafi","year":"2014","journal-title":"Neuron"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.cell.2009.08.027","article-title":"Stringent specificity in the construction of a GABAergic presynaptic inhibitory circuit","volume":"139","author":"Betley","year":"2009","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"2614","DOI":"10.1016\/j.celrep.2020.01.102","article-title":"Glia Promote Synaptogenesis through an IQGAP PES-7 in C. elegans","volume":"30","author":"Dong","year":"2020","journal-title":"Cell Rep."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1083\/jcb.201110127","article-title":"Netrin instructs synaptic vesicle clustering through Rac GTPase, MIG-10, and the actin cytoskeleton","volume":"197","author":"Stavoe","year":"2012","journal-title":"J. Cell Biol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1126\/science.aau8977","article-title":"Distinct molecular programs regulate synapse specificity in cortical inhibitory circuits","volume":"363","author":"Favuzzi","year":"2019","journal-title":"Science"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"3831","DOI":"10.1083\/jcb.201703042","article-title":"Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly","volume":"216","author":"Anderson","year":"2017","journal-title":"J. Cell Biol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"eaav7969","DOI":"10.1126\/science.aav7969","article-title":"Latrophilin GPCRs direct synapse specificity by coincident binding of FLRTs and teneurins","volume":"363","author":"Sando","year":"2019","journal-title":"Science"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/j.neuron.2018.06.026","article-title":"A Modular Organization of LRR Protein-Mediated Synaptic Adhesion Defines Synapse Identity","volume":"99","author":"Schroeder","year":"2018","journal-title":"Neuron"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"e57000","DOI":"10.7554\/eLife.57000","article-title":"Subcellular sorting of neuregulins controls the assembly of excitatory-inhibitory cortical circuits","volume":"9","author":"Bernard","year":"2020","journal-title":"eLife"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1057","DOI":"10.1038\/35074025","article-title":"Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse","volume":"410","author":"Lin","year":"2001","journal-title":"Nature"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/S0896-6273(01)00287-2","article-title":"Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation","volume":"30","author":"Yang","year":"2001","journal-title":"Neuron"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1126\/science.287.5450.131","article-title":"DNA topoisomerase IIbeta and neural development","volume":"287","author":"Yang","year":"2000","journal-title":"Science"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/nn2026","article-title":"MuSK controls where motor axons grow and form synapses","volume":"11","author":"Kim","year":"2008","journal-title":"Nat. Neurosci."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.conb.2017.05.005","article-title":"mRNA transport & local translation in neurons","volume":"45","author":"Glock","year":"2017","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1038\/s41594-019-0263-5","article-title":"Local translation in neurons: Visualization and function","volume":"26","author":"Holt","year":"2019","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"7131","DOI":"10.1523\/JNEUROSCI.1801-06.2006","article-title":"RNA trafficking and local protein synthesis in dendrites: An overview","volume":"26","author":"Martin","year":"2006","journal-title":"J. Neurosci."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.neuroscience.2017.05.025","article-title":"Neuronal activity patterns in the developing barrel cortex","volume":"368","author":"Luhmann","year":"2018","journal-title":"Neuroscience"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1093\/oxfordjournals.schbul.a006880","article-title":"Early Brain Wiring: Activity-Dependent Processes","volume":"27","author":"Penn","year":"2001","journal-title":"Schizophr. Bull."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1038\/nature05300","article-title":"Electrical activity in early neuronal development","volume":"444","author":"Spitzer","year":"2006","journal-title":"Nature"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1038\/nrn.2017.30","article-title":"Genetic and activity-dependent mechanisms underlying interneuron diversity","volume":"18","author":"Wamsley","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.pneurobio.2005.06.003","article-title":"BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis","volume":"76","author":"Bramham","year":"2005","journal-title":"Prog. Neurobiol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"2730","DOI":"10.1152\/jn.00616.2016","article-title":"Developmental experience-dependent plasticity in the first synapse of the Drosophila olfactory circuit","volume":"116","author":"Golovin","year":"2016","journal-title":"J. Neurophysiol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.conb.2018.08.014","article-title":"State-dependent plasticity of innate behavior in fruit flies","volume":"54","year":"2019","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1016\/j.bbagrm.2007.12.010","article-title":"Roles of ubiquitination at the synapse","volume":"1779","author":"Haas","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/nature25192","article-title":"Neurexin controls plasticity of a mature, sexually dimorphic neuron","volume":"553","author":"Hart","year":"2018","journal-title":"Nature"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.conb.2018.06.013","article-title":"Synaptic plasticity in human cortical circuits: Cellular mechanisms of learning and memory in the human brain?","volume":"54","author":"Mansvelder","year":"2019","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1038\/nrn2303","article-title":"Synaptic plasticity, memory and the hippocampus: A neural network approach to causality","volume":"9","author":"Neves","year":"2008","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1016\/j.neuron.2007.10.035","article-title":"Activity-dependent plasticity in an olfactory circuit","volume":"56","author":"Sachse","year":"2007","journal-title":"Neuron"},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1242\/dev.127.6.1253","article-title":"A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction","volume":"127","author":"Zhao","year":"2000","journal-title":"Development"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1038\/nature12743","article-title":"The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition","volume":"503","author":"Bloodgood","year":"2013","journal-title":"Nature"},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Wang, M., Witvliet, D., Wu, M., Kang, L., and Shao, Z. (2021). Temperature regulates synaptic subcellular specificity mediated by inhibitory glutamate signaling. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009295"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.conb.2017.08.017","article-title":"The diverse actions of astrocytes during synaptic development","volume":"47","author":"Bosworth","year":"2017","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_125","doi-asserted-by":"crossref","unstructured":"Farizatto, K.L.G., and Baldwin, K.T. (2023). Astrocyte-synapse interactions during brain development. Curr. Opin. Neurobiol., 80.","DOI":"10.1016\/j.conb.2023.102704"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.cell.2013.06.028","article-title":"Synapse location during growth depends on glia location","volume":"154","author":"Shao","year":"2013","journal-title":"Cell"},{"key":"ref_127","doi-asserted-by":"crossref","unstructured":"Ango, F., Wu, C., Van der Want, J.J., Wu, P., Schachner, M., Huang, Z.J., and Ghosh, A. (2008). Bergmann Glia and the Recognition Molecule CHL1 Organize GABAergic Axons and Direct Innervation of Purkinje Cell Dendrites. PLoS Biol., 6.","DOI":"10.1371\/journal.pbio.0060103"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"e30809","DOI":"10.7554\/eLife.30809","article-title":"The role of microglia and their CX3CR1 signaling in adult neurogenesis in the olfactory bulb","volume":"6","author":"Reshef","year":"2017","journal-title":"eLife"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"2283","DOI":"10.1523\/JNEUROSCI.3751-14.2015","article-title":"Axon initial segment-associated microglia","volume":"35","author":"Baalman","year":"2015","journal-title":"J. Neurosci."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"4048","DOI":"10.1016\/j.cell.2021.06.018","article-title":"GABA-receptive microglia selectively sculpt developing inhibitory circuits","volume":"184","author":"Favuzzi","year":"2021","journal-title":"Cell"},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"e55890","DOI":"10.7554\/eLife.55890","article-title":"A muscle-epidermis-glia signaling axis sustains synaptic specificity during allometric growth in Caenorhabditis elegans","volume":"9","author":"Fan","year":"2020","journal-title":"eLife"},{"key":"ref_132","unstructured":"The C. elegans Research Community (2005). Epidermal morphogenesis. WormBook, WormBook Research Community."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1002\/wdev.79","article-title":"The Caenorhabditis elegans epidermis as a model skin. I: Development, patterning, and growth","volume":"1","author":"Chisholm","year":"2012","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/bs.ctdb.2015.11.012","article-title":"elegans Embryonic Morphogenesis","volume":"116","author":"Yang","year":"2016","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"e53267","DOI":"10.15252\/embr.202153267","article-title":"Gut neuroendocrine signaling regulates synaptic assembly in C. elegans","volume":"23","author":"Shi","year":"2022","journal-title":"EMBO Rep."},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.conb.2019.01.025","article-title":"Compartmentalized distributions of neuronal and glial cell-surface proteins pattern the synaptic network","volume":"57","year":"2019","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.conb.2017.11.005","article-title":"Building stereotypic connectivity: Mechanistic insights into structural plasticity from C. elegans","volume":"48","author":"Jin","year":"2018","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"e1129486","DOI":"10.1080\/21624054.2015.1129486","article-title":"Neural circuit rewiring: Insights from DD synapse remodeling","volume":"5","author":"Kurup","year":"2016","journal-title":"Worm"}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/14\/2\/155\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:53:59Z","timestamp":1760104439000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/14\/2\/155"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,2]]},"references-count":138,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2024,2]]}},"alternative-id":["brainsci14020155"],"URL":"https:\/\/doi.org\/10.3390\/brainsci14020155","relation":{},"ISSN":["2076-3425"],"issn-type":[{"value":"2076-3425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,2]]}}}