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Brockman Research Fellowship in Child Development"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Int. J. Mol. Sci.","IJMS"],"abstract":"<jats:p>Interactions among molecular recognition systems, neuronal activity, and glial regulation transform early neuronal connectivity into precise functional circuits during brain development. The cerebellum is a powerful model for studying these mechanisms due to its stereotyped and accessible circuitry. Two major excitatory afferent pathways\u2014climbing fibers (CFs), which convey error-related signals to Purkinje cells (PCs), and mossy fibers (MFs), which transmit sensorimotor information via granule cells (GCs) and parallel fibers (PFs)\u2014undergo strengthening, competition, and refinement during postnatal development. Synaptic specificity is established by general and pathway-specific organizers. The neurexin\u2013neuroligin system broadly regulates synapse formation, while the neurexin\u2013CBLN1\u2013GluD2 complex specifies PF\u2013PC synapses and C1qL1\u2013BAI3 signaling stabilizes the dominant CF input during competitive refinement. CF\u2013PC synapse elimination serves as a classic model of activity-dependent competition, where weaker inputs are removed through calcium-dependent mechanisms. In parallel, glial cells regulate synaptic maturation: microglia shape inhibitory environments, and Bergmann glia support glutamate homeostasis, dendritic organization, and synapse stability. PCs integrate CF and PF inputs and provide inhibitory output to the cerebellar nuclei, where convergent excitatory collaterals from CFs and MFs are combined with PC inhibition to generate cerebellar output. Together, these coordinated molecular, cellular, and circuit-level mechanisms establish the synaptic architecture underlying cerebellar computation, motor coordination, and adaptive learning, which are the central focus of this review.<\/jats:p>","DOI":"10.3390\/ijms27177576","type":"journal-article","created":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T14:49:34Z","timestamp":1787582974000},"page":"7576","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Molecular and Cellular Mechanisms of Synaptogenesis and Synaptic Refinement During Cerebellar Circuit Formation"],"prefix":"10.3390","volume":"27","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8090-4795","authenticated-orcid":false,"given":"Farshid","family":"Ghiyamihoor","sequence":"first","affiliation":[{"name":"Department of Human Anatomy and Cell Science, Rady Faculty of Health Sciences, Max Rady College of Medicine, University of Manitoba, Winnipeg, MB R3E 0J9, Canada"},{"name":"The Children\u2019s Hospital Research Institute of Manitoba (CHRIM), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB R3E 3P4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Azam","family":"Asemi Rad","sequence":"additional","affiliation":[{"name":"Department of Human Anatomy and Cell Science, Rady Faculty of Health Sciences, Max Rady College of Medicine, University of Manitoba, Winnipeg, MB R3E 0J9, Canada"},{"name":"The Children\u2019s Hospital Research Institute of Manitoba (CHRIM), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB R3E 3P4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6885-2590","authenticated-orcid":false,"given":"Hassan","family":"Marzban","sequence":"additional","affiliation":[{"name":"Department of Human Anatomy and Cell Science, Rady Faculty of Health Sciences, Max Rady College of Medicine, University of Manitoba, Winnipeg, MB R3E 0J9, Canada"},{"name":"The Children\u2019s Hospital Research Institute of Manitoba (CHRIM), Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, MB R3E 3P4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s12311-024-01778-8","article-title":"Causally Mapping the Cerebellum in Children and Young Adults: From Motor to Cognition","volume":"24","author":"Veyrie","year":"2025","journal-title":"Cerebellum"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s12311-013-0511-x","article-title":"Consensus paper: The cerebellum\u2019s role in movement and cognition","volume":"13","author":"Koziol","year":"2014","journal-title":"Cerebellum"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"141","DOI":"10.25259\/SNI_226_2024","article-title":"Redefining cerebellar assessment: A comprehensive review of the cerebellum\u2019s cognitive and affective roles and the efficacy of CCAS scales","volume":"15","author":"Alan","year":"2024","journal-title":"Surg. Neurol. Int."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"7554","DOI":"10.1523\/JNEUROSCI.1451-23.2023","article-title":"Cognitive-Affective Functions of the Cerebellum","volume":"43","author":"Rudolph","year":"2023","journal-title":"J. Neurosci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1126\/science.aax7526","article-title":"Spatiotemporal expansion of primary progenitor zones in the developing human cerebellum","volume":"366","author":"Haldipur","year":"2019","journal-title":"Science"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1159\/000519068","article-title":"Time in Neurogenesis: Conservation of the Developmental Formation of the Cerebellar Circuitry","volume":"97","year":"2022","journal-title":"Brain Behav. Evol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Galas, L., B\u00e9nard, M., Lebon, A., Komuro, Y., Schapman, D., Vaudry, H., Vaudry, D., and Komuro, H. (2017). Postnatal Migration of Cerebellar Interneurons. Brain Sci., 7.","DOI":"10.3390\/brainsci7060062"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"RP93778","DOI":"10.7554\/eLife.93778.4","article-title":"Identification of an early subset of cerebellar nuclei neurons in mice","volume":"13","author":"Amiri","year":"2024","journal-title":"eLife"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1007\/s12311-025-01848-5","article-title":"The Nuclear Transitory Zone: A Key Player in the Cerebellar Development","volume":"24","author":"Ghiyamihoor","year":"2025","journal-title":"Cerebellum"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1159\/000350503","article-title":"Sequence of synaptogenesis in the fetal and neonatal cerebellar system\u2014Part 1: Guillain-Mollaret triangle (dentato-rubro-olivo-cerebellar circuit)","volume":"35","author":"Sarnat","year":"2013","journal-title":"Dev. Neurosci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3441","DOI":"10.1113\/jphysiol.2010.201582","article-title":"The mysterious microcircuitry of the cerebellar nuclei","volume":"589","author":"Uusisaari","year":"2011","journal-title":"J. Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Mishina, M., Uemura, T., Yasumura, M., and Yoshida, T. (2012). Molecular mechanism of parallel fiber-Purkinje cell synapse formation. Front. Neural Circuits, 6.","DOI":"10.3389\/fncir.2012.00090"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1007\/s12311-018-0964-z","article-title":"Multiple Phases of Climbing Fiber Synapse Elimination in the Developing Cerebellum","volume":"17","author":"Kano","year":"2018","journal-title":"Cerebellum"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2830","DOI":"10.1038\/s41467-018-05100-z","article-title":"Microglia permit climbing fiber elimination by promoting GABAergic inhibition in the developing cerebellum","volume":"9","author":"Nakayama","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"7438","DOI":"10.1073\/pnas.1617330114","article-title":"Glutamate transporter GLAST controls synaptic wrapping by Bergmann glia and ensures proper wiring of Purkinje cells","volume":"114","author":"Miyazaki","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"eado3927","DOI":"10.1126\/science.ado3927","article-title":"Cross-species single-cell spatial transcriptomic atlases of the cerebellar cortex","volume":"385","author":"Hao","year":"2024","journal-title":"Science"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1146\/annurev-neuro-111020-091953","article-title":"Human Cerebellar Development and Transcriptomics: Implications for Neurodevelopmental Disorders","volume":"45","author":"Haldipur","year":"2022","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1038\/s41586-023-06884-x","article-title":"Cellular development and evolution of the mammalian cerebellum","volume":"625","author":"Sepp","year":"2024","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"9146","DOI":"10.1038\/s41467-025-64204-5","article-title":"Co-Conservation of synaptic gene expression and circuitry in collicular neurons","volume":"16","author":"Liu","year":"2025","journal-title":"Nat. Commun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"a003079","DOI":"10.1101\/cshperspect.a003079","article-title":"Cell adhesion, the backbone of the synapse: \u201cvertebrate\u201d and \u201cinvertebrate\u201d perspectives","volume":"1","author":"Giagtzoglou","year":"2009","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1038\/nn.3276","article-title":"Synaptic scaffold evolution generated components of vertebrate cognitive complexity","volume":"16","author":"Nithianantharajah","year":"2013","journal-title":"Nat. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1146\/annurev-neuro-062012-170307","article-title":"Genetic approaches to neural circuits in the mouse","volume":"36","author":"Huang","year":"2013","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Mudge, J., Miller, N.A., Khrebtukova, I., Lindquist, I.E., May, G.D., Huntley, J.J., Luo, S., Zhang, L., van Velkinburgh, J.C., and Farmer, A.D. (2008). Genomic convergence analysis of schizophrenia: mRNA sequencing reveals altered synaptic vesicular transport in post-mortem cerebellum. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0003625"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/nn.2719","article-title":"Characterization of the proteome, diseases and evolution of the human postsynaptic density","volume":"14","author":"Collins","year":"2011","journal-title":"Nat. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.neuron.2019.05.002","article-title":"SynGO: An Evidence-Based, Expert-Curated Knowledge Base for the Synapse","volume":"103","author":"Koopmans","year":"2019","journal-title":"Neuron"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3149","DOI":"10.1093\/brain\/awu281","article-title":"Abnormal climbing fibre-Purkinje cell synaptic connections in the essential tremor cerebellum","volume":"137","author":"Lin","year":"2014","journal-title":"Brain"},{"key":"ref_27","first-page":"362","article-title":"Synaptic Pruning by Microglia: Lessons from Genetic Studies in Mice","volume":"47","author":"Nandi","year":"2025","journal-title":"Dev. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1177\/01926233211046933","article-title":"Comparative Milestones in Rodent and Human Postnatal Central Nervous System Development","volume":"49","author":"Zeiss","year":"2021","journal-title":"Toxicol. Pathol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1111\/jnc.12001","article-title":"Differential neurite outgrowth is required for axon specification by cultured hippocampal neurons","volume":"123","author":"Yamamoto","year":"2012","journal-title":"J. Neurochem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1007\/s00441-014-1955-0","article-title":"Cytoskeletal and signaling mechanisms of neurite formation","volume":"359","author":"Sainath","year":"2015","journal-title":"Cell Tissue Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"a001925","DOI":"10.1101\/cshperspect.a001925","article-title":"Initiating and growing an axon","volume":"2","author":"Polleux","year":"2010","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e12387","DOI":"10.7554\/eLife.12387","article-title":"Waves of actin and microtubule polymerization drive microtubule-based transport and neurite growth before single axon formation","volume":"5","author":"Winans","year":"2016","journal-title":"Elife"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1038\/nrm2679","article-title":"The trip of the tip: Understanding the growth cone machinery","volume":"10","author":"Lowery","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1016\/j.neuron.2012.03.005","article-title":"Growth cone travel in space and time: The cellular ensemble of cytoskeleton, adhesion, and membrane","volume":"73","author":"Vitriol","year":"2012","journal-title":"Neuron"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/0896-6273(91)90360-C","article-title":"Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs","volume":"6","author":"Doherty","year":"1991","journal-title":"Neuron"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1093\/cercor\/bhg110","article-title":"The role of L1 in axon pathfinding and fasciculation","volume":"14","author":"Bartsch","year":"2004","journal-title":"Cereb. Cortex"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"16502","DOI":"10.1073\/pnas.1114028108","article-title":"The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo","volume":"108","author":"Fuccillo","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1186\/gb-2013-14-9-213","article-title":"Neurexins","volume":"14","author":"Reissner","year":"2013","journal-title":"Genome Biol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Qi, C., Luo, L.D., Feng, I., and Ma, S. (2022). Molecular mechanisms of synaptogenesis. Front. Synaptic Neurosci., 14.","DOI":"10.3389\/fnsyn.2022.939793"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.neuron.2018.09.040","article-title":"Towards an Understanding of Synapse Formation","volume":"100","year":"2018","journal-title":"Neuron"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.neuron.2020.01.003","article-title":"LRRTMs Organize Synapses through Differential Engagement of Neurexin and PTP\u03c3","volume":"106","author":"Roppongi","year":"2020","journal-title":"Neuron"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"8807","DOI":"10.1038\/s41467-024-53090-y","article-title":"LRRTM2 controls presynapse nano-organization and AMPA receptor sub-positioning through Neurexin-binding interface","volume":"15","author":"Liouta","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"7495","DOI":"10.1523\/JNEUROSCI.0470-10.2010","article-title":"LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development","volume":"30","author":"Siddiqui","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"4057","DOI":"10.1073\/pnas.1209881110","article-title":"Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases","volume":"110","author":"Yim","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e202103052","DOI":"10.1083\/jcb.202103052","article-title":"The cell biology of synapse formation","volume":"220","year":"2021","journal-title":"J. Cell Biol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Cooper, J.N., Mittal, J., Sangadi, A., Klassen, D.L., King, A.M., Zalta, M., Mittal, R., and Eshraghi, A.A. (2024). Landscape of NRXN1 Gene Variants in Phenotypic Manifestations of Autism Spectrum Disorder: A Systematic Review. J. Clin. Med., 13.","DOI":"10.3390\/jcm13072067"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41525-024-00450-8","article-title":"Analysis of exonic deletions in a large population study provides novel insights into NRXN1 pathology","volume":"9","author":"Montalbano","year":"2024","journal-title":"npj Genom. Med."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Nguyen, T.A., Lehr, A.W., and Roche, K.W. (2020). Neuroligins and Neurodevelopmental Disorders: X-Linked Genetics. Front. Synaptic Neurosci., 12.","DOI":"10.3389\/fnsyn.2020.00033"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"eabd8379","DOI":"10.1126\/scisignal.abd8379","article-title":"Neuroligin-2 as a central organizer of inhibitory synapses in health and disease","volume":"13","author":"Ali","year":"2020","journal-title":"Sci. Signal"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e70292","DOI":"10.1111\/jnc.70292","article-title":"Synaptic and Non-Synaptic Functions of PTPRD: A Receptor Tyrosine Phosphatase at the Crossroads of Neural Circuitry and Metabolism","volume":"169","author":"Kim","year":"2025","journal-title":"J. Neurochem."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/s40659-024-00522-0","article-title":"Loss of protein tyrosine phosphatase receptor delta PTPRD increases the number of cortical neurons, impairs synaptic function and induces autistic-like behaviors in adult mice","volume":"57","author":"Meza","year":"2024","journal-title":"Biol. Res."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"4415","DOI":"10.1038\/s41467-025-59685-3","article-title":"Alternatively spliced mini-exon B in PTP\u03b4 regulates excitatory synapses through cell-type-specific trans-synaptic PTP\u03b4-IL1RAP interaction","volume":"16","author":"Kim","year":"2025","journal-title":"Nat. Commun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.tins.2008.07.001","article-title":"Cadherins and catenins at synapses: Roles in synaptogenesis and synaptic plasticity","volume":"31","author":"Arikkath","year":"2008","journal-title":"Trends Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3297","DOI":"10.1242\/dev.090621","article-title":"Clustered protocadherins","volume":"140","author":"Chen","year":"2013","journal-title":"Development"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"13479","DOI":"10.1073\/pnas.0702334104","article-title":"\u03b2-Catenin regulates excitatory postsynaptic strength at hippocampal synapses","volume":"104","author":"Okuda","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"943","DOI":"10.1002\/hipo.22282","article-title":"N-cadherin regulates molecular organization of excitatory and inhibitory synaptic circuits in adult hippocampus in vivo","volume":"24","author":"Nikitczuk","year":"2014","journal-title":"Hippocampus"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"6892","DOI":"10.1523\/JNEUROSCI.18-17-06892.1998","article-title":"N-cadherin redistribution during synaptogenesis in hippocampal neurons","volume":"18","author":"Benson","year":"1998","journal-title":"J. Neurosci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1617","DOI":"10.1523\/JNEUROSCI.11-06-01617.1991","article-title":"The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture","volume":"11","author":"Fletcher","year":"1991","journal-title":"J. Neurosci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1159\/000351031","article-title":"Synaptogenesis in the foetal and neonatal cerebellar system. 2. Pontine nuclei and cerebellar cortex","volume":"35","author":"Sarnat","year":"2013","journal-title":"Dev. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1007\/s10571-019-00683-7","article-title":"Decreased Expression of Synaptophysin 1 (SYP1 Major Synaptic Vesicle Protein p38) and Contactin 6 (CNTN6\/NB3) in the Cerebellar Vermis of reln Haplodeficient Mice","volume":"39","author":"Castagna","year":"2019","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"a005678","DOI":"10.1101\/cshperspect.a005678","article-title":"The postsynaptic organization of synapses","volume":"3","author":"Sheng","year":"2011","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"E6983","DOI":"10.1073\/pnas.1517045112","article-title":"PSD-95 family MAGUKs are essential for anchoring AMPA and NMDA receptor complexes at the postsynaptic density","volume":"112","author":"Chen","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1186\/gb-2007-8-2-206","article-title":"The Homer family proteins","volume":"8","author":"Furuichi","year":"2007","journal-title":"Genome Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/ng1933","article-title":"Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders","volume":"39","author":"Durand","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/nrn.2016.183","article-title":"SHANK proteins: Roles at the synapse and in autism spectrum disorder","volume":"18","author":"Monteiro","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"27491","DOI":"10.1038\/srep27491","article-title":"Resequencing and Association Analysis of Six PSD-95-Related Genes as Possible Susceptibility Genes for Schizophrenia and Autism Spectrum Disorders","volume":"6","author":"Xing","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Levy, A.M., Gomez-Puertas, P., and T\u00fcmer, Z. (2022). Neurodevelopmental Disorders Associated with PSD-95 and Its Interaction Partners. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23084390"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1176\/appi.ajp.2010.10040484","article-title":"Association of mouse Dlg4 (PSD-95) gene deletion and human DLG4 gene variation with phenotypes relevant to autism spectrum disorders and Williams\u2019 syndrome","volume":"167","author":"Feyder","year":"2010","journal-title":"Am. J. Psychiatry"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"8293","DOI":"10.1038\/s41467-025-63748-w","article-title":"Gephyrin filaments represent the molecular basis of inhibitory postsynaptic densities","volume":"16","author":"Macha","year":"2025","journal-title":"Nat. Commun."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1038\/s41422-020-00440-2","article-title":"Gephyrin: A scaffold that builds a phase at the inhibitory postsynapses","volume":"31","author":"Hoffmann","year":"2021","journal-title":"Cell Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1016\/j.neuron.2009.08.023","article-title":"Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin","volume":"63","author":"Poulopoulos","year":"2009","journal-title":"Neuron"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"5935","DOI":"10.1113\/JP286400","article-title":"The synaptic vesicle cluster as a controller of pre- and postsynaptic structure and function","volume":"603","author":"Reshetniak","year":"2025","journal-title":"J. Physiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1523\/JNEUROSCI.4733-03.2004","article-title":"Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity","volume":"24","author":"Ehrlich","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"E3131","DOI":"10.1073\/pnas.1506488112","article-title":"Progressive maturation of silent synapses governs the duration of a critical period","volume":"112","author":"Huang","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.mcn.2009.05.004","article-title":"Neuroligin-2 accelerates GABAergic synapse maturation in cerebellar granule cells","volume":"42","author":"Fu","year":"2009","journal-title":"Mol. Cell. Neurosci."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1111\/j.1469-7793.2000.t01-1-00299.x","article-title":"Slow deactivation kinetics of NMDA receptors containing NR1 and NR2D subunits in rat cerebellar Purkinje cells","volume":"525","author":"Misra","year":"2000","journal-title":"J. Physiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1113\/jphysiol.2007.141531","article-title":"Climbing-fibre activation of NMDA receptors in Purkinje cells of adult mice","volume":"585","author":"Renzi","year":"2007","journal-title":"J. Physiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"10797","DOI":"10.1523\/JNEUROSCI.2422-07.2007","article-title":"NMDA receptor contribution to the climbing fiber response in the adult mouse Purkinje cell","volume":"27","author":"Piochon","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"15330","DOI":"10.1523\/JNEUROSCI.4344-10.2010","article-title":"Purkinje cell NMDA receptors assume a key role in synaptic gain control in the mature cerebellum","volume":"30","author":"Piochon","year":"2010","journal-title":"J. Neurosci."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Liu, H., Lan, Y., Bing, Y.H., Chu, C.P., and Qiu, D.L. (2016). N-methyl-D-Aspartate Receptors Contribute to Complex Spike Signaling in Cerebellar Purkinje Cells: An In vivo Study in Mice. Front. Cell. Neurosci., 10.","DOI":"10.3389\/fncel.2016.00172"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"11593","DOI":"10.1073\/pnas.200354297","article-title":"Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse","volume":"97","author":"Casado","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/s41583-021-00507-y","article-title":"Mechanisms governing activity-dependent synaptic pruning in the developing mammalian CNS","volume":"22","author":"Faust","year":"2021","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1146\/annurev.neuro.24.1.139","article-title":"Synaptic modification by correlated activity: Hebb\u2019s postulate revisited","volume":"24","author":"Bi","year":"2001","journal-title":"Annu. Rev. Neurosci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1177\/10738584231170167","article-title":"Activity-Dependent Synapse Refinement: From Mechanisms to Molecules","volume":"30","author":"Burbridge","year":"2024","journal-title":"Neuroscientist"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"113093","DOI":"10.1016\/j.isci.2025.113093","article-title":"Synaptic pruning following NMDAR-dependent LTD preferentially affects isolated synapses","volume":"28","author":"Camus","year":"2025","journal-title":"iScience"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.nlm.2016.10.013","article-title":"Long-term depression-associated signaling is required for an in vitro model of NMDA receptor-dependent synapse pruning","volume":"138","author":"Henson","year":"2017","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1038\/nn.4389","article-title":"LTD-like molecular pathways in developmental synaptic pruning","volume":"19","author":"Piochon","year":"2016","journal-title":"Nat. Neurosci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1146\/annurev.cellbio.24.110707.175235","article-title":"Communication between the synapse and the nucleus in neuronal development, plasticity, and disease","volume":"24","author":"Cohen","year":"2008","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1177\/1073858418769644","article-title":"Dendritic Spine Elimination: Molecular Mechanisms and Implications","volume":"25","author":"Stein","year":"2019","journal-title":"Neuroscientist"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1101\/lm.54603","article-title":"BDNF and activity-dependent synaptic modulation","volume":"10","author":"Lu","year":"2003","journal-title":"Learn. Mem."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"102692","DOI":"10.1016\/j.conb.2023.102692","article-title":"The molecular signals that regulate activity-dependent synapse refinement in the brain","volume":"79","author":"Yasuda","year":"2023","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1016\/j.neuron.2021.03.006","article-title":"An activity-dependent determinant of synapse elimination in the mammalian brain","volume":"109","author":"Yasuda","year":"2021","journal-title":"Neuron"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1002\/glia.24650","article-title":"Microglia and Astrocytes in Postnatal Neural Circuit Formation","volume":"73","author":"Duffy","year":"2025","journal-title":"Glia"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1456","DOI":"10.1126\/science.1202529","article-title":"Synaptic pruning by microglia is necessary for normal brain development","volume":"333","author":"Paolicelli","year":"2011","journal-title":"Science"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"102877","DOI":"10.1016\/j.conb.2024.102877","article-title":"Microglia phagocytic mechanisms: Development informing disease","volume":"86","author":"Beiter","year":"2024","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1016\/j.neuron.2012.03.026","article-title":"Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner","volume":"74","author":"Schafer","year":"2012","journal-title":"Neuron"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1016\/j.cell.2007.10.036","article-title":"The classical complement cascade mediates CNS synapse elimination","volume":"131","author":"Stevens","year":"2007","journal-title":"Cell"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1111\/jnc.15689","article-title":"Microglia-dependent remodeling of neuronal circuits","volume":"163","author":"Guedes","year":"2022","journal-title":"J. Neurochem."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1126\/science.aal3589","article-title":"Astrocyte-derived interleukin-33 promotes microglial synapse engulfment and neural circuit development","volume":"359","author":"Vainchtein","year":"2018","journal-title":"Science"},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Lee, E., and Chung, W.S. (2019). Glial Control of Synapse Number in Healthy and Diseased Brain. Front. Cell. Neurosci., 13.","DOI":"10.3389\/fncel.2019.00042"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1038\/nature12776","article-title":"Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways","volume":"504","author":"Chung","year":"2013","journal-title":"Nature"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1002\/glia.24145","article-title":"Phagocytic astrocytes: Emerging from the shadows of microglia","volume":"70","author":"Konishi","year":"2022","journal-title":"Glia"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"5185","DOI":"10.1523\/JNEUROSCI.3850-15.2016","article-title":"Megf10 Is a Receptor for C1Q That Mediates Clearance of Apoptotic Cells by Astrocytes","volume":"36","author":"Iram","year":"2016","journal-title":"J. Neurosci."},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Nelson, N., Miller, V., and Broadie, K. (2025). Neuron-to-glia and glia-to-glia signaling directs critical period experience-dependent synapse pruning. Front. Cell Dev. Biol., 13.","DOI":"10.3389\/fcell.2025.1540052"},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Xu, W., L\u00f6wel, S., and Schl\u00fcter, O.M. (2020). Silent Synapse-Based Mechanisms of Critical Period Plasticity. Front. Cell. Neurosci., 14.","DOI":"10.3389\/fncel.2020.00213"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1186\/s13041-025-01261-3","article-title":"Perineuronal nets in the developing brain: Implications for neurodevelopmental disorders","volume":"18","author":"Ackerman","year":"2025","journal-title":"Mol. Brain"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"7071","DOI":"10.1073\/pnas.1817222116","article-title":"Structural maturation of cortical perineuronal nets and their perforating synapses revealed by superresolution imaging","volume":"116","author":"Sigal","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.tins.2019.04.003","article-title":"Perineuronal Nets: Plasticity, Protection, and Therapeutic Potential","volume":"42","author":"Reichelt","year":"2019","journal-title":"Trends Neurosci."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1038\/nrn1787","article-title":"Critical period plasticity in local cortical circuits","volume":"6","author":"Hensch","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1126\/science.1072699","article-title":"Reactivation of ocular dominance plasticity in the adult visual cortex","volume":"298","author":"Pizzorusso","year":"2002","journal-title":"Science"},{"key":"ref_111","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_112","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.conb.2011.01.009","article-title":"The metamorphosis of the developing cerebellar microcircuit","volume":"21","author":"Smith","year":"2011","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"2121","DOI":"10.1007\/s00429-019-01897-7","article-title":"Merlin modulates process outgrowth and synaptogenesis in the cerebellum","volume":"224","author":"Toledo","year":"2019","journal-title":"Brain Struct. Funct."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/s40673-015-0026-y","article-title":"Embryonic stages in cerebellar afferent development","volume":"2","author":"Afsharinezhad","year":"2015","journal-title":"Cerebellum Ataxias"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/s00429-011-0339-4","article-title":"Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2","volume":"217","author":"Gebre","year":"2012","journal-title":"Brain Struct. Funct."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1007\/s12311-022-01388-2","article-title":"Early Cerebellar Development in Relation to the Trigeminal System","volume":"21","author":"Marzban","year":"2022","journal-title":"Cerebellum"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"2421","DOI":"10.1007\/s00429-019-01916-7","article-title":"Early trigeminal ganglion afferents enter the cerebellum before the Purkinje cells are born and target the nuclear transitory zone","volume":"224","author":"Marzban","year":"2019","journal-title":"Brain Struct. Funct."},{"key":"ref_118","doi-asserted-by":"crossref","unstructured":"Kalinovsky, A., Boukhtouche, F., Blazeski, R., Bornmann, C., Suzuki, N., Mason, C.A., and Scheiffele, P. (2011). Development of axon-target specificity of ponto-cerebellar afferents. PLoS Biol., 9.","DOI":"10.1371\/journal.pbio.1001013"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1007\/s12311-015-0712-6","article-title":"Mossy Fibers Terminate Directly within Purkinje Cell Zones During Mouse Development","volume":"15","author":"Sillitoe","year":"2016","journal-title":"Cerebellum"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/0306-4522(89)90110-3","article-title":"Transient direct connection of vestibular mossy fibers to the vestibulocerebellar Purkinje cells in early postnatal development of kittens","volume":"32","author":"Takeda","year":"1989","journal-title":"Neuroscience"},{"key":"ref_121","doi-asserted-by":"crossref","unstructured":"White, J.J., and Sillitoe, R.V. (2013). Postnatal development of cerebellar zones revealed by neurofilament heavy chain protein expression. Front. Neuroanat., 7.","DOI":"10.3389\/fnana.2013.00009"},{"key":"ref_122","doi-asserted-by":"crossref","unstructured":"Lackey, E.P., and Sillitoe, R.V. (2020). Eph\/ephrin Function Contributes to the Patterning of Spinocerebellar Mossy Fibers into Parasagittal Zones. Front. Syst. Neurosci., 14.","DOI":"10.3389\/fnsys.2020.00007"},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Marzban, H., Del Bigio, M.R., Alizadeh, J., Ghavami, S., Zachariah, R.M., and Rastegar, M. (2014). Cellular commitment in the developing cerebellum. Front. Cell. Neurosci., 8.","DOI":"10.3389\/fncel.2014.00450"},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"12782","DOI":"10.1073\/pnas.0906653106","article-title":"Dendrites of cerebellar granule cells correctly recognize their target axons for synaptogenesis in vitro","volume":"106","author":"Ito","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1038\/s42003-023-04825-y","article-title":"Developmental timing-dependent organization of synaptic connections between mossy fibers and granule cells in the cerebellum","volume":"6","author":"Kim","year":"2023","journal-title":"Commun. Biol."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1083\/jcb.200511054","article-title":"Signaling across the synapse: A role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release","volume":"174","author":"Ciani","year":"2006","journal-title":"J. Cell Biol."},{"key":"ref_127","first-page":"219","article-title":"Neurodevelopmental Perspectives on Wnt Signaling in Psychiatry","volume":"2","author":"Mulligan","year":"2017","journal-title":"Mol. Neuropsychiatry"},{"key":"ref_128","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_129","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_130","doi-asserted-by":"crossref","unstructured":"Teo, S., and Salinas, P.C. (2021). Wnt-Frizzled Signaling Regulates Activity-Mediated Synapse Formation. Front. Mol. Neurosci., 14.","DOI":"10.3389\/fnmol.2021.683035"},{"key":"ref_131","doi-asserted-by":"crossref","unstructured":"Kim, M., Jun, S., Park, H., Tanaka-Yamamoto, K., and Yamamoto, Y. (2023). Regulation of cerebellar network development by granule cells and their molecules. Front. Mol. Neurosci., 16.","DOI":"10.3389\/fnmol.2023.1236015"},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"1408","DOI":"10.1200\/JCO.2009.27.4324","article-title":"Medulloblastoma comprises four distinct molecular variants","volume":"29","author":"Northcott","year":"2011","journal-title":"J. Clin. Oncol."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1586\/ern.12.66","article-title":"Molecular subgroups of medulloblastoma","volume":"12","author":"Northcott","year":"2012","journal-title":"Expert. Rev. Neurother."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.cell.2004.06.025","article-title":"FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain","volume":"118","author":"Umemori","year":"2004","journal-title":"Cell"},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"523","DOI":"10.4161\/cam.4.4.12733","article-title":"Neural circuit formation in the cerebellum is controlled by cell adhesion molecules of the Contactin family","volume":"4","author":"Stoeckli","year":"2010","journal-title":"Cell Adhes. Migr."},{"key":"ref_136","doi-asserted-by":"crossref","unstructured":"Masoli, S., Rizza, M.F., Moccia, F., and D\u2019Angelo, E. (2025). The spiny relationship between parallel fibers, climbing fibers, and Purkinje cells. Front. Physiol., 16.","DOI":"10.3389\/fphys.2025.1671271"},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1080\/14734220310011407","article-title":"Axonal varicosity distributions along parallel fibers: A new angle on a cerebellar circuit","volume":"2","author":"Shepherd","year":"2003","journal-title":"Cerebellum"},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.neuron.2020.11.028","article-title":"GluD2- and Cbln1-mediated competitive interactions shape the dendritic arbors of cerebellar Purkinje cells","volume":"109","author":"Takeo","year":"2021","journal-title":"Neuron"},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"1534","DOI":"10.1038\/nn1576","article-title":"Cbln1 is essential for synaptic integrity and plasticity in the cerebellum","volume":"8","author":"Hirai","year":"2005","journal-title":"Nat. Neurosci."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1126\/science.1185152","article-title":"Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer","volume":"328","author":"Matsuda","year":"2010","journal-title":"Science"},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1111\/jnc.12022","article-title":"A complex of synaptic adhesion molecule CADM1, a molecule related to autism spectrum disorder, with MUPP1 in the cerebellum","volume":"123","author":"Fujita","year":"2012","journal-title":"J. Neurochem."},{"key":"ref_142","doi-asserted-by":"crossref","unstructured":"Fujita, E., Tanabe, Y., Imhof, B.A., Momoi, M.Y., and Momoi, T. (2012). Cadm1-expressing synapses on Purkinje cell dendrites are involved in mouse ultrasonic vocalization activity. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030151"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1002\/dneu.20742","article-title":"Contribution of the neural cell recognition molecule NB-3 to synapse formation between parallel fibers and Purkinje cells in mouse","volume":"69","author":"Sakurai","year":"2009","journal-title":"Dev. Neurobiol."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"3435","DOI":"10.1016\/j.neuron.2023.09.031","article-title":"IL-4 shapes microglia-dependent pruning of the cerebellum during postnatal development","volume":"111","author":"Guedes","year":"2023","journal-title":"Neuron"},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.brainresrev.2010.10.001","article-title":"The unipolar brush cell: A remarkable neuron finally receiving deserved attention","volume":"66","author":"Mugnaini","year":"2011","journal-title":"Brain Res. Rev."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"4403","DOI":"10.1113\/jphysiol.2011.216572","article-title":"Cerebellar Golgi cell inhibition gets slowly more complicated","volume":"589","author":"Houston","year":"2011","journal-title":"J. Physiol."},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"13099","DOI":"10.1073\/pnas.1510249112","article-title":"Control of cerebellar granule cell output by sensory-evoked Golgi cell inhibition","volume":"112","author":"Duguid","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"12430","DOI":"10.1523\/JNEUROSCI.4897-11.2013","article-title":"Granule cell ascending axon excitatory synapses onto Golgi cells implement a potent feedback circuit in the cerebellar granular layer","volume":"33","author":"Cesana","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_149","doi-asserted-by":"crossref","unstructured":"D\u2019Angelo, E., Solinas, S., Mapelli, J., Gandolfi, D., Mapelli, L., and Prestori, F. (2013). The cerebellar Golgi cell and spatiotemporal organization of granular layer activity. Front. Neural Circuits, 7.","DOI":"10.3389\/fncir.2013.00093"},{"key":"ref_150","doi-asserted-by":"crossref","first-page":"2239","DOI":"10.1111\/j.1460-9568.2007.05846.x","article-title":"GABAergic synaptogenesis marks the onset of differentiation of basket and stellate cells in mouse cerebellum","volume":"26","author":"Simat","year":"2007","journal-title":"Eur. J. Neurosci."},{"key":"ref_151","doi-asserted-by":"crossref","first-page":"3837","DOI":"10.1113\/jphysiol.2011.207167","article-title":"Multiple extra-synaptic spillover mechanisms regulate prolonged activity in cerebellar Golgi cell-granule cell loops","volume":"589","author":"Holtzman","year":"2011","journal-title":"J. Physiol."},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"e29215","DOI":"10.7554\/eLife.29215","article-title":"Non-synaptic signaling from cerebellar climbing fibers modulates Golgi cell activity","volume":"6","author":"Nietz","year":"2017","journal-title":"Elife"},{"key":"ref_153","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1016\/S0896-6273(03)00530-0","article-title":"mGluR2 postsynaptically senses granule cell inputs at Golgi cell synapses","volume":"39","author":"Watanabe","year":"2003","journal-title":"Neuron"},{"key":"ref_154","doi-asserted-by":"crossref","unstructured":"Okuno, Y., Sakoori, K., Matsuyama, K., Yamasaki, M., Watanabe, M., Hashimoto, K., Watanabe, T., and Kano, M. (2023). PTP\u03b4 is a presynaptic organizer for the formation and maintenance of climbing fiber to Purkinje cell synapses in the developing cerebellum. Front. Mol. Neurosci., 16.","DOI":"10.3389\/fnmol.2023.1206245"},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"2849","DOI":"10.1016\/j.celrep.2019.10.081","article-title":"Developmental Rewiring between Cerebellar Climbing Fibers and Purkinje Cells Begins with Positive Feedback Synapse Addition","volume":"29","author":"Wilson","year":"2019","journal-title":"Cell Rep."},{"key":"ref_156","doi-asserted-by":"crossref","first-page":"9987","DOI":"10.1073\/pnas.1101488108","article-title":"Postsynaptic P\/Q-type Ca2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum","volume":"108","author":"Hashimoto","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_157","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1016\/S0896-6273(03)00298-8","article-title":"Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum","volume":"38","author":"Hashimoto","year":"2003","journal-title":"Neuron"},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"2732","DOI":"10.1038\/ncomms3732","article-title":"Spike timing-dependent selective strengthening of single climbing fibre inputs to Purkinje cells during cerebellar development","volume":"4","author":"Kawamura","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_159","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1056\/NEJM200107053450103","article-title":"The clinical spectrum of familial hemiplegic migraine associated with mutations in a neuronal calcium channel","volume":"345","author":"Ducros","year":"2001","journal-title":"N. Engl. J. Med."},{"key":"ref_160","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/s10048-004-0183-2","article-title":"A G301R Na+\/K+ -ATPase mutation causes familial hemiplegic migraine type 2 with cerebellar signs","volume":"5","author":"Spadaro","year":"2004","journal-title":"Neurogenetics"},{"key":"ref_161","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.1111\/j.1526-4610.2009.01464.x","article-title":"CACNA1A nonsense mutation is associated with basilar-type migraine and episodic ataxia type 2","volume":"49","author":"Robbins","year":"2009","journal-title":"Headache"},{"key":"ref_162","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1001\/archneur.60.4.610","article-title":"Phenotypes of spinocerebellar ataxia type 6 and familial hemiplegic migraine caused by a unique CACNA1A missense mutation in patients from a large family","volume":"60","author":"Alonso","year":"2003","journal-title":"Arch. Neurol."},{"key":"ref_163","doi-asserted-by":"crossref","first-page":"e2416797122","DOI":"10.1073\/pnas.2416797122","article-title":"Synaptic transmission is dispensable for selecting the winner input but is crucial for the subsequent events of synapse elimination","volume":"122","author":"Kao","year":"2025","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_164","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.neuron.2009.06.008","article-title":"Translocation of a \u201cwinner\u201d climbing fiber to the Purkinje cell dendrite and subsequent elimination of \u201closers\u201d from the soma in developing cerebellum","volume":"63","author":"Hashimoto","year":"2009","journal-title":"Neuron"},{"key":"ref_165","doi-asserted-by":"crossref","first-page":"7641","DOI":"10.1523\/JNEUROSCI.4561-12.2013","article-title":"Dendritic translocation establishes the winner in cerebellar climbing fiber synapse elimination","volume":"33","author":"Carrillo","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1002\/dneu.20730","article-title":"Differential expression of TrkB isoforms switches climbing fiber-Purkinje cell synaptogenesis to selective synapse elimination","volume":"69","author":"Sherrard","year":"2009","journal-title":"Dev. Neurobiol."},{"key":"ref_167","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1038\/87419","article-title":"Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum","volume":"4","author":"Hansel","year":"2001","journal-title":"Nat. Neurosci."},{"key":"ref_168","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1152\/physrev.2001.81.3.1143","article-title":"Cerebellar long-term depression: Characterization, signal transduction, and functional roles","volume":"81","author":"Ito","year":"2001","journal-title":"Physiol. Rev."},{"key":"ref_169","doi-asserted-by":"crossref","first-page":"9701","DOI":"10.1523\/JNEUROSCI.21-24-09701.2001","article-title":"Roles of glutamate receptor delta 2 subunit (GluRdelta 2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development","volume":"21","author":"Hashimoto","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_170","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/nn.2329","article-title":"\u03b2CaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses","volume":"12","author":"Hoebeek","year":"2009","journal-title":"Nat. Neurosci."},{"key":"ref_171","doi-asserted-by":"crossref","first-page":"10768","DOI":"10.1523\/JNEUROSCI.2876-05.2005","article-title":"A role for protein phosphatases 1, 2A, and 2B in cerebellar long-term potentiation","volume":"25","author":"Belmeguenai","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_172","doi-asserted-by":"crossref","unstructured":"Pinto, T.M., Schilstra, M.J., Steuber, V., and Roque, A.C. (2014). \u03b2CaMKII regulates bidirectional long-term plasticity in cerebellar Purkinje cells by a CaMKII\/PP2B switch mechanism. BMC Neurosci., 15.","DOI":"10.1186\/1471-2202-15-S1-P58"},{"key":"ref_173","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1038\/s41467-017-00260-w","article-title":"Retrograde BDNF to TrkB signaling promotes synapse elimination in the developing cerebellum","volume":"8","author":"Choo","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_174","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1126\/science.1252514","article-title":"Retrograde semaphorin signaling regulates synapse elimination in the developing mouse brain","volume":"344","author":"Uesaka","year":"2014","journal-title":"Science"},{"key":"ref_175","doi-asserted-by":"crossref","first-page":"15724","DOI":"10.1073\/pnas.95.26.15724","article-title":"Phospholipase cbeta4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum","volume":"95","author":"Kano","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_176","doi-asserted-by":"crossref","first-page":"4954","DOI":"10.1523\/JNEUROSCI.20-13-04954.2000","article-title":"Critical period for activity-dependent synapse elimination in developing cerebellum","volume":"20","author":"Kakizawa","year":"2000","journal-title":"J. Neurosci."},{"key":"ref_177","doi-asserted-by":"crossref","first-page":"e2425460123","DOI":"10.1073\/pnas.2425460123","article-title":"mGluR1 signaling is necessary for strengthening winner climbing fiber inputs in the developing mouse cerebellum","volume":"123","author":"Yamasaki","year":"2026","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_178","doi-asserted-by":"crossref","first-page":"2282","DOI":"10.1073\/pnas.1511513113","article-title":"Territories of heterologous inputs onto Purkinje cell dendrites are segregated by mGluR1-dependent parallel fiber synapse elimination","volume":"113","author":"Ichikawa","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_179","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1016\/j.neuron.2018.01.018","article-title":"Retrograde Signaling from Progranulin to Sort1 Counteracts Synapse Elimination in the Developing Cerebellum","volume":"97","author":"Uesaka","year":"2018","journal-title":"Neuron"},{"key":"ref_180","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.neuron.2014.12.020","article-title":"Anterograde C1ql1 signaling is required in order to determine and maintain a single-winner climbing fiber in the mouse cerebellum","volume":"85","author":"Kakegawa","year":"2015","journal-title":"Neuron"},{"key":"ref_181","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1016\/j.celrep.2015.01.034","article-title":"The Secreted Protein C1QL1 and Its Receptor BAI3 Control the Synaptic Connectivity of Excitatory Inputs Converging on Cerebellar Purkinje Cells","volume":"10","author":"Sigoillot","year":"2015","journal-title":"Cell Rep."},{"key":"ref_182","doi-asserted-by":"crossref","first-page":"114427","DOI":"10.1016\/j.celrep.2024.114427","article-title":"Kainate receptors regulate synaptic integrity and plasticity by forming a complex with synaptic organizers in the cerebellum","volume":"43","author":"Kakegawa","year":"2024","journal-title":"Cell Rep."},{"key":"ref_183","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/s13041-023-01048-4","article-title":"C1ql1-Bai3 signaling is necessary for climbing fiber synapse formation in mature Purkinje cells in coordination with neuronal activity","volume":"16","author":"Aimi","year":"2023","journal-title":"Mol. Brain"},{"key":"ref_184","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1126\/science.adi1024","article-title":"Climbing fiber multi-innervation of mouse Purkinje dendrites with arborization common to human","volume":"381","author":"Busch","year":"2023","journal-title":"Science"},{"key":"ref_185","doi-asserted-by":"crossref","first-page":"RP105013","DOI":"10.7554\/eLife.105013","article-title":"Non-allometric expansion and enhanced compartmentalization of Purkinje cell dendrites in the human cerebellum","volume":"14","author":"Busch","year":"2025","journal-title":"eLife"},{"key":"ref_186","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.bpsgos.2021.09.004","article-title":"Sensory Over-responsivity and Aberrant Plasticity in Cerebellar Cortex in a Mouse Model of Syndromic Autism","volume":"2","author":"Simmons","year":"2022","journal-title":"Biol. Psychiatry Glob. Open Sci."},{"key":"ref_187","doi-asserted-by":"crossref","first-page":"1378","DOI":"10.1212\/WNL.0b013e3182a841a3","article-title":"Deletions in GRID2 lead to a recessive syndrome of cerebellar ataxia and tonic upgaze in humans","volume":"81","author":"Hills","year":"2013","journal-title":"Neurology"},{"key":"ref_188","doi-asserted-by":"crossref","first-page":"926","DOI":"10.1177\/0883073813484967","article-title":"A homozygous deletion in GRID2 causes a human phenotype with cerebellar ataxia and atrophy","volume":"28","author":"Utine","year":"2013","journal-title":"J. Child. Neurol."},{"key":"ref_189","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1038\/s41439-022-00204-x","article-title":"A heterozygous GRID2 mutation in autosomal dominant cerebellar ataxia","volume":"9","author":"Koh","year":"2022","journal-title":"Hum. Genome Var."},{"key":"ref_190","doi-asserted-by":"crossref","first-page":"1751","DOI":"10.1212\/WNL.0000000000001524","article-title":"GRID2 mutations span from congenital to mild adult-onset cerebellar ataxia","volume":"84","author":"Coutelier","year":"2015","journal-title":"Neurology"},{"key":"ref_191","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1093\/hmg\/ddad188","article-title":"Clinical features, functional consequences, and rescue pharmacology of missense GRID1 and GRID2 human variants","volume":"33","author":"Allen","year":"2024","journal-title":"Hum. Mol. Genet."},{"key":"ref_192","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1007\/s12311-025-01837-8","article-title":"Spinocerebellar Ataxia 44 Caused by a Novel GRM1 Variant: Reviewing the Contrasting Pathogenic Mechanisms Underlying Two GRM1-Associated Hereditary Ataxias","volume":"24","author":"Lan","year":"2025","journal-title":"Cerebellum"},{"key":"ref_193","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.ajhg.2017.08.005","article-title":"Dominant Mutations in GRM1 Cause Spinocerebellar Ataxia Type 44","volume":"101","author":"Watson","year":"2017","journal-title":"Am. J. Hum. Genet."},{"key":"ref_194","doi-asserted-by":"crossref","first-page":"1768","DOI":"10.1007\/s12311-023-01617-2","article-title":"Severe Neurodevelopmental Disorder in Autosomal Recessive Spinocerebellar Ataxia 13 (SCAR13) Caused by Two Novel Frameshift Variants in GRM1","volume":"23","author":"Cesaroni","year":"2024","journal-title":"Cerebellum"},{"key":"ref_195","doi-asserted-by":"crossref","first-page":"1749","DOI":"10.1001\/archneur.60.12.1749","article-title":"Spinocerebellar ataxia type 14 caused by a mutation in protein kinase C gamma","volume":"60","author":"Yabe","year":"2003","journal-title":"Arch. Neurol."},{"key":"ref_196","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1136\/jnnp.2004.044115","article-title":"Spinocerebellar ataxia type 14: Study of a family with an exon 5 mutation in the PRKCG gene","volume":"76","author":"Fahey","year":"2005","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_197","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/s41431-018-0321-1","article-title":"Biallelic intragenic duplication in ADGRB3 (BAI3) gene associated with intellectual disability, cerebellar atrophy, and behavioral disorder","volume":"27","author":"Scuderi","year":"2019","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_198","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/j.tins.2021.04.001","article-title":"Little cells of the little brain: Microglia in cerebellar development and function","volume":"44","author":"Stoessel","year":"2021","journal-title":"Trends Neurosci."},{"key":"ref_199","doi-asserted-by":"crossref","first-page":"2316","DOI":"10.1002\/glia.23842","article-title":"Undisturbed climbing fiber pruning in the cerebellar cortex of CX(3) CR1-deficient mice","volume":"68","author":"Kaiser","year":"2020","journal-title":"Glia"},{"key":"ref_200","doi-asserted-by":"crossref","first-page":"1742","DOI":"10.1038\/s41598-018-38264-1","article-title":"Molecular layer interneurons shape the spike activity of cerebellar Purkinje cells","volume":"9","author":"Brown","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_201","doi-asserted-by":"crossref","unstructured":"Sasso\u00e8-Pognetto, M., Frola, E., Pregno, G., Briatore, F., and Patrizi, A. (2011). Understanding the molecular diversity of GABAergic synapses. Front. Cell. Neurosci., 5.","DOI":"10.3389\/fncel.2011.00004"},{"key":"ref_202","doi-asserted-by":"crossref","unstructured":"Ango, F., Wu, C., Van der Want, J.J., Wu, P., Schachner, M., and Huang, Z.J. (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_203","doi-asserted-by":"crossref","first-page":"13151","DOI":"10.1073\/pnas.0802390105","article-title":"Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors","volume":"105","author":"Patrizi","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_204","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1111\/j.1460-9568.2009.06975.x","article-title":"IL1RAPL1 controls inhibitory networks during cerebellar development in mice","volume":"30","author":"Gambino","year":"2009","journal-title":"Eur. J. Neurosci."},{"key":"ref_205","doi-asserted-by":"crossref","first-page":"5691","DOI":"10.1113\/jphysiol.2013.259499","article-title":"HCN1 channels in cerebellar Purkinje cells promote late stages of learning and constrain synaptic inhibition","volume":"591","author":"Rinaldi","year":"2013","journal-title":"J. Physiol."},{"key":"ref_206","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/S0092-8674(03)00884-5","article-title":"The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells","volume":"115","author":"Nolan","year":"2003","journal-title":"Cell"},{"key":"ref_207","doi-asserted-by":"crossref","first-page":"25192","DOI":"10.1038\/s41598-025-09964-2","article-title":"Cerebellar basket cell filtering of Purkinje cell responses elicited by low frequency parallel fibre transmission","volume":"15","author":"Masoli","year":"2025","journal-title":"Sci. Rep."},{"key":"ref_208","doi-asserted-by":"crossref","first-page":"1837","DOI":"10.1523\/JNEUROSCI.20-05-01837.2000","article-title":"Serotonin-driven long-range inhibitory connections in the cerebellar cortex","volume":"20","author":"Dumoulin","year":"2000","journal-title":"J. Neurosci."},{"key":"ref_209","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.neuron.2016.05.037","article-title":"Purkinje Cell Collaterals Enable Output Signals from the Cerebellar Cortex to Feed Back to Purkinje Cells and Interneurons","volume":"91","author":"Witter","year":"2016","journal-title":"Neuron"},{"key":"ref_210","doi-asserted-by":"crossref","first-page":"4457","DOI":"10.1523\/JNEUROSCI.23-11-04457.2003","article-title":"Serotonin drives a novel GABAergic synaptic current recorded in rat cerebellar purkinje cells: A Lugaro cell to Purkinje cell synapse","volume":"23","author":"Dean","year":"2003","journal-title":"J. Neurosci."},{"key":"ref_211","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/1749-8104-5-23","article-title":"Migration, early axonogenesis, and Reelin-dependent layer-forming behavior of early\/posterior-born Purkinje cells in the developing mouse lateral cerebellum","volume":"5","author":"Miyata","year":"2010","journal-title":"Neural Dev."},{"key":"ref_212","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/S0306-4522(01)00127-0","article-title":"The development of inhibitory synaptic specializations in the mouse deep cerebellar nuclei","volume":"105","author":"Garin","year":"2001","journal-title":"Neuroscience"},{"key":"ref_213","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1002\/cne.10226","article-title":"Distribution of postsynaptic GABA(A) receptor aggregates in the deep cerebellar nuclei of normal and mutant mice","volume":"447","author":"Garin","year":"2002","journal-title":"J. Comp. Neurol."},{"key":"ref_214","doi-asserted-by":"crossref","first-page":"1022","DOI":"10.1038\/s41598-018-19314-0","article-title":"Myelination of Purkinje axons is critical for resilient synaptic transmission in the deep cerebellar nucleus","volume":"8","author":"Barron","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_215","doi-asserted-by":"crossref","unstructured":"Matsuno, H., Kudoh, M., Watakabe, A., Yamamori, T., Shigemoto, R., and Nagao, S. (2016). Distribution and Structure of Synapses on Medial Vestibular Nuclear Neurons Targeted by Cerebellar Flocculus Purkinje Cells and Vestibular Nerve in Mice: Light and Electron Microscopy Studies. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0164037"},{"key":"ref_216","doi-asserted-by":"crossref","first-page":"6392","DOI":"10.1523\/JNEUROSCI.23-15-06392.2003","article-title":"Purkinje cell synapses target physiologically unique brainstem neurons","volume":"23","author":"Sekirnjak","year":"2003","journal-title":"J. Neurosci."},{"key":"ref_217","first-page":"3","article-title":"Cerebello-vestibular connections of the anterior vermis. A retrograde tracer study in different mammals including primates","volume":"129","author":"Voogd","year":"1991","journal-title":"Arch. Ital. Biol."},{"key":"ref_218","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1007\/s12311-022-01506-0","article-title":"Cerebellum Lecture: The Cerebellar Nuclei-Core of the Cerebellum","volume":"23","author":"Kebschull","year":"2024","journal-title":"Cerebellum"},{"key":"ref_219","doi-asserted-by":"crossref","first-page":"5245","DOI":"10.1113\/JP274321","article-title":"Facilitation of mossy fibre-driven spiking in the cerebellar nuclei by the synchrony of inhibition","volume":"595","author":"Wu","year":"2017","journal-title":"J. Physiol."},{"key":"ref_220","first-page":"981","article-title":"Climbing fibre collaterals contact neurons in the cerebellar nuclei that provide a GABAergic feedback to the inferior olive","volume":"80","author":"Hawkins","year":"1997","journal-title":"Neuroscience"},{"key":"ref_221","doi-asserted-by":"crossref","first-page":"6703","DOI":"10.1113\/JP274598","article-title":"Synaptic excitation by climbing fibre collaterals in the cerebellar nuclei of juvenile and adult mice","volume":"595","author":"Najac","year":"2017","journal-title":"J. Physiol."},{"key":"ref_222","doi-asserted-by":"crossref","first-page":"6589","DOI":"10.1113\/JP275091","article-title":"Collateral impact: A dual role for climbing fibre collaterals to the cerebellar nuclei?","volume":"595","author":"Pickford","year":"2017","journal-title":"J. Physiol."},{"key":"ref_223","doi-asserted-by":"crossref","unstructured":"Bengtsson, F., and J\u00f6rntell, H. (2014). Specific relationship between excitatory inputs and climbing fiber receptive fields in deep cerebellar nuclear neurons. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0084616"},{"key":"ref_224","doi-asserted-by":"crossref","first-page":"1848","DOI":"10.1016\/j.neuron.2024.02.014","article-title":"Simple spike patterns and synaptic mechanisms encoding sensory and motor signals in Purkinje cells and the cerebellar nuclei","volume":"112","author":"Brown","year":"2024","journal-title":"Neuron"},{"key":"ref_225","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1038\/nature10732","article-title":"Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei","volume":"481","author":"Person","year":"2011","journal-title":"Nature"},{"key":"ref_226","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1007\/s12311-011-0261-6","article-title":"Control of cerebellar nuclear cells: A direct role for complex spikes?","volume":"10","author":"Lang","year":"2011","journal-title":"Cerebellum"},{"key":"ref_227","doi-asserted-by":"crossref","first-page":"9826","DOI":"10.1523\/JNEUROSCI.2069-09.2009","article-title":"Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei","volume":"29","author":"Zheng","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_228","doi-asserted-by":"crossref","first-page":"1697","DOI":"10.1152\/jn.1999.82.4.1697","article-title":"Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum","volume":"82","author":"Aizenman","year":"1999","journal-title":"J. Neurophysiol."},{"key":"ref_229","doi-asserted-by":"crossref","first-page":"5555","DOI":"10.1073\/pnas.0601261103","article-title":"Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons","volume":"103","author":"Molineux","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_230","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0896-6273(03)00802-X","article-title":"Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites","volume":"41","author":"Telgkamp","year":"2004","journal-title":"Neuron"},{"key":"ref_231","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1523\/JNEUROSCI.3583-14.2015","article-title":"Integration of Purkinje cell inhibition by cerebellar nucleo-olivary neurons","volume":"35","author":"Najac","year":"2015","journal-title":"J. Neurosci."},{"key":"ref_232","doi-asserted-by":"crossref","first-page":"9418","DOI":"10.1523\/JNEUROSCI.0401-14.2014","article-title":"Differential GABAergic and glycinergic inputs of inhibitory interneurons and Purkinje cells to principal cells of the cerebellar nuclei","volume":"34","author":"Husson","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_233","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1002\/cne.20822","article-title":"Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components","volume":"494","author":"Carulli","year":"2006","journal-title":"J. Comp. Neurol."},{"key":"ref_234","doi-asserted-by":"crossref","first-page":"1721","DOI":"10.1002\/cne.23009","article-title":"Bral2 is indispensable for the proper localization of brevican and the structural integrity of the perineuronal net in the brainstem and cerebellum","volume":"520","author":"Bekku","year":"2012","journal-title":"J. Comp. Neurol."},{"key":"ref_235","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1007\/s12311-025-01920-0","article-title":"Characterization of Perineuronal Nets in the Human Cerebellum","volume":"24","author":"Mpai","year":"2025","journal-title":"Cerebellum"},{"key":"ref_236","doi-asserted-by":"crossref","unstructured":"Schreurs, B.G., O\u2019Dell, D.E., and Wang, D. (2024). The Role of Cerebellar Intrinsic Neuronal Excitability, Synaptic Plasticity, and Perineuronal Nets in Eyeblink Conditioning. Biology, 13.","DOI":"10.3390\/biology13030200"},{"key":"ref_237","first-page":"1313","article-title":"Ablation of Projection Glutamatergic Neurons in the Lateral Cerebellar Nuclei Alters Motor Coordination in Vglut2-Cre+ Mice","volume":"23","author":"Ghiyamihoor","year":"2024","journal-title":"Cerebellum"},{"key":"ref_238","doi-asserted-by":"crossref","first-page":"e58613","DOI":"10.7554\/eLife.58613","article-title":"Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis","volume":"9","author":"Fujita","year":"2020","journal-title":"eLife"},{"key":"ref_239","doi-asserted-by":"crossref","unstructured":"Dumas, D.B., Gornati, S.V., Adolfs, Y., Shimogori, T., Pasterkamp, R.J., and Hoebeek, F.E. (2022). Anatomical Development of the Cerebellothalamic Tract in Embryonic Mice. Cells, 11.","DOI":"10.3390\/cells11233800"},{"key":"ref_240","doi-asserted-by":"crossref","unstructured":"Bohne, P., Schwarz, M.K., Herlitze, S., and Mark, M.D. (2019). A New Projection From the Deep Cerebellar Nuclei to the Hippocampus via the Ventrolateral and Laterodorsal Thalamus in Mice. Front. Neural Circuits, 13.","DOI":"10.3389\/fncir.2019.00051"},{"key":"ref_241","doi-asserted-by":"crossref","first-page":"eadp2377","DOI":"10.1126\/sciadv.adp2377","article-title":"Aberrant outputs of glutamatergic neurons in deep cerebellar nuclei mediate dystonic movements","volume":"11","author":"Wu","year":"2025","journal-title":"Sci. Adv."},{"key":"ref_242","doi-asserted-by":"crossref","first-page":"e61672","DOI":"10.7554\/eLife.61672","article-title":"Cerebellar and vestibular nuclear synapses in the inferior olive have distinct release kinetics and neurotransmitters","volume":"9","author":"Turecek","year":"2020","journal-title":"eLife"},{"key":"ref_243","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/0006-8993(88)91142-0","article-title":"A new combination of WGA-HRP anterograde tracing and GABA immunocytochemistry applied to afferents of the cat inferior olive at the ultrastructural level","volume":"447","author":"Holstege","year":"1988","journal-title":"Brain Res."},{"key":"ref_244","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1038\/s41593-023-01387-4","article-title":"Excitatory nucleo-olivary pathway shapes cerebellar outputs for motor control","volume":"26","author":"Wang","year":"2023","journal-title":"Nat. Neurosci."},{"key":"ref_245","doi-asserted-by":"crossref","first-page":"e66231","DOI":"10.7554\/eLife.66231","article-title":"Diverse inhibitory projections from the cerebellar interposed nucleus","volume":"10","author":"Judd","year":"2021","journal-title":"eLife"},{"key":"ref_246","doi-asserted-by":"crossref","first-page":"10104","DOI":"10.1523\/JNEUROSCI.2087-09.2009","article-title":"Glycinergic projection neurons of the cerebellum","volume":"29","author":"Bagnall","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_247","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1007\/s12311-009-0137-1","article-title":"GlyT2+ neurons in the lateral cerebellar nucleus","volume":"9","author":"Uusisaari","year":"2010","journal-title":"Cerebellum"},{"key":"ref_248","doi-asserted-by":"crossref","unstructured":"Robinson, K., Delhaye, M., and Craig, A.M. (2024). Mapping proteomic composition of excitatory postsynaptic sites in the cerebellar cortex. Front. Mol. Neurosci., 17.","DOI":"10.3389\/fnmol.2024.1381534"},{"key":"ref_249","doi-asserted-by":"crossref","unstructured":"Ibrahimi, M., Gray, M.T., Rochon, P.-L., Eiras, S.M., Pietraszkiewicz, P., Dabiri, S., Hicks, J.L., Salter, M.W., Boisvert, M., and Paquet, M.-E. (2026). TRACR: An anterograde transneuronal tracing system for genetic access across synapses and longitudinal circuit analysis. bioRxiv, preprint.","DOI":"10.64898\/2026.02.08.704659"},{"key":"ref_250","doi-asserted-by":"crossref","unstructured":"Ajongbolo, A.O., and Langhans, S.A. (2025). Brain Organoids and Assembloids\u2014From Disease Modeling to Drug Discovery. 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