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We integrated postmortem retinal and matched brain histopathology with ultrastructural, proteomic, biochemical, and machine\u2010learning analyses across cognitively normal, mild cognitive impairment, and AD cohorts. Retinal glutamatergic synapses exhibited early, progressive degeneration, marked by loss of presynaptic vesicular glutamate transporter 1 (VGLUT1) and synaptophysin\u00a0and\u00a0postsynaptic density protein 95 (PSD95) and N\u2010methyl\u2010D\u2010aspartate receptor subunit 2A (NMDAR2A), along with ribbon synapse ultrastructural disruption. Synaptic deficits correlated with amyloid\u2010\u03b2\n                    <jats:sub>42<\/jats:sub>\n                    (A\u03b2\n                    <jats:sub>42<\/jats:sub>\n                    ), pathogenic tau, oxidative stress, the A\u03b2\u2010binding p75 neurotrophin receptor, and glial activation that paralleled disease progression. Proteomics revealed widespread synaptic remodeling accompanied by disease\u2010associated microglia, astrocyte\u2010mediated excitotoxicity, and pyroptotic pathways. The synapse\u2010enriched deubiquitinase ubiquitin C\u2010terminal hydrolase L1 (UCHL1) was dysregulated early, particularly in horizontal and bipolar interneurons, and strongly associated with synaptic loss and neuroinflammation. Mechanistically, fibrillar A\u03b2\n                    <jats:sub>42<\/jats:sub>\n                    induced rapid UCHL1 and synaptic depletion in human and murine neurons before overt neurodegeneration. Machine\u2010learning models identified retinal UCHL1 as the strongest predictor of Braak stage and cognitive impairment. These findings establish the retina as an early site of AD synaptopathy and position UCHL1 as a candidate biomarker and mechanistic mediator linking amyloid pathology, neuroinflammation, and synaptic vulnerability.\n                  <\/jats:p>","DOI":"10.1002\/advs.202600020","type":"journal-article","created":{"date-parts":[[2026,8,29]],"date-time":"2026-08-29T07:12:56Z","timestamp":1787987576000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Early Retinal UCHL1 Dysregulation Coupled With Synaptic Loss Reflects Alzheimer's Disease Severity"],"prefix":"10.1002","author":[{"given":"Altan","family":"Rentsendorj","sequence":"first","affiliation":[{"name":"Department of Neurosurgery Maxine Dunitz Neurosurgical Institute Cedars\u2010Sinai Medical Center  Los Angeles California 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Cedars\u2010Sinai Medical Center  Los Angeles California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edward","family":"Robinson","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery Maxine Dunitz Neurosurgical Institute Cedars\u2010Sinai Medical Center  Los Angeles California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ernesto","family":"Barron","sequence":"additional","affiliation":[{"name":"Doheny Eye Institute University of California  Los Angeles California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony","family":"Rodriguez","sequence":"additional","affiliation":[{"name":"Doheny Eye Institute University of California  Los Angeles California USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ousman","family":"Jallow","sequence":"additional","affiliation":[{"name":"Department of Neurosurgery Maxine Dunitz Neurosurgical Institute Cedars\u2010Sinai Medical Center  Los 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