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The failure of recovery of synaptic function is due to excitotoxic injury. We hypothesized that changes in mitochondrial metabolism contribute to the heightened vulnerability to excitotoxicity in the synGLT\u20101 KO mice. We found impaired flux of carbon from\n                    <jats:sup>13<\/jats:sup>\n                    C\u2010glucose into the tricarboxylic acid cycle in synGLT\u20101 KO cortical and hippocampal slices compared with wild\u2010type (WT) slices. In addition, we found downregulation of the neuronal glucose transporter GLUT3 in both genotypes. Flux of carbon from [1,2\u2010\n                    <jats:sup>13<\/jats:sup>\n                    C]acetate, thought to be astrocyte\u2010specific, was increased in the synGLT\u2010KO hippocampal slices but not cortical slices. Glycogen stores, predominantly localized to astrocytes, are rapidly depleted in slices after cutting, and are replenished during ex\u00a0vivo incubation. In the synGLT\u20101 KO, replenishment of glycogen stores during ex\u00a0vivo incubation was compromised. These results suggest both neuronal and astrocytic metabolic perturbations in the synGLT\u20101 KO slices. Supplementing incubation medium during recovery with 20\u2009mM D\u2010glucose normalized glycogen replenishment but had no effect on recovery of synaptic function. In contrast, 20\u2009mM non\u2010metabolizable L\u2010glucose substantially improved recovery of synaptic function, suggesting that D\u2010glucose metabolism contributes to the excitotoxic injury in the synGLT\u20101 KO slices. L\u2010lactate substitution for D\u2010glucose did not promote recovery of synaptic function, implicating mitochondrial metabolism. Consistent with this hypothesis, phosphorylation of pyruvate dehydrogenase, which decreases enzyme activity, was increased in WT slices during the recovery period, but not in synGLT\u20101 KO slices. Since metabolism of glucose by the mitochondrial electron transport chain is associated with superoxide production, we tested the effect of drugs that scavenge and prevent superoxide production. The superoxide dismutase\/catalase mimic EUK\u2010134 conferred complete protection and full recovery of synaptic function. A site\u2010specific inhibitor of complex III superoxide production, S3QEL\u20102, was also protective, but inhibitors of NADPH oxidase were not. In summary, we find that the failure of recovery of synaptic function in hippocampal slices from the synGLT\u20101 KO mouse, previously shown to be due to excitotoxic injury, is caused by production of superoxide by mitochondrial metabolism.\n                    <jats:boxed-text content-type=\"graphic\" position=\"anchor\">\n                      <jats:graphic xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" mimetype=\"image\/png\" position=\"anchor\" specific-use=\"enlarged-web-image\" xlink:href=\"graphic\/jnc16205-fig-0008-m.png\">\n                        <jats:alt-text>image<\/jats:alt-text>\n                      <\/jats:graphic>\n                    <\/jats:boxed-text>\n                  <\/jats:p>","DOI":"10.1111\/jnc.16205","type":"journal-article","created":{"date-parts":[[2024,8,28]],"date-time":"2024-08-28T05:31:13Z","timestamp":1724823073000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Misprogramming of glucose metabolism impairs recovery of hippocampal slices from neuronal GLT\u20101 knockout mice and contributes to excitotoxic injury through mitochondrial superoxide production"],"prefix":"10.1111","volume":"169","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9451-2151","authenticated-orcid":false,"given":"S.","family":"Li","sequence":"first","affiliation":[{"name":"Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital Harvard Medical School  Boston Massachusetts USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neurology, F.M. Kirby Neurobiology Center, Boston Children's Hospital Harvard Medical School  Boston Massachusetts USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8767-2675","authenticated-orcid":false,"given":"J. V.","family":"Andersen","sequence":"additional","affiliation":[{"name":"Department of Drug Design and Pharmacology, Faculty of Health and Medical Sciences University of Copenhagen  Copenhagen Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5027-1218","authenticated-orcid":false,"given":"B. 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