{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T19:51:23Z","timestamp":1792525883437,"version":"4.5.0"},"reference-count":125,"publisher":"SAGE Publications","issue":"s1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JAD"],"published-print":{"date-parts":[[2021,6,22]]},"abstract":"<jats:p>Background: Normal aging is accompanied by cognitive deficiencies, affecting women and men equally. Aging is the main risk factor for Alzheimer\u2019s disease (AD), with women having a higher risk. The higher prevalence of AD in women is associated with the abrupt hormonal decline seen after menopause. However, other factors may be involved in this sex-related cognitive decline. Alterations in gut microbiota (GM) and its bioproducts have been reported in AD subjects and transgenic (Tg) mice, having a direct impact on brain amyloid-\u03b2 pathology in male (M), but not in female (F) mice. Objective: The aim of this work was to determine GM composition and cognitive dysfunction in M and F wildtype (WT) and Tg mice, in a sex\/genotype segregation design. Methods: Anxiety, short term working-memory, spatial learning, and long-term spatial memory were evaluated in 6-month-old WT and Tg male mice. Fecal short chain fatty acids were determined by chromatography, and DNA sequencing and bioinformatic analyses were used to determine GM differences. Results: We observed sex-dependent differences in cognitive skills in WT mice, favoring F mice. However, the cognitive advantage of females was lost in Tg mice. GM composition showed few sex-related differences in WT mice. Contrary, Tg-M mice presented a more severe dysbiosis than Tg-F mice. A decreased abundance of Ruminococcaceae was associated with cognitive deficits in Tg-F mice, while butyrate levels were positively associated with better working- and object recognition-memory in WT-F mice. Conclusion: This report describes a sex-dependent association between GM alterations and cognitive impairment in a mice model of AD.<\/jats:p>","DOI":"10.3233\/jad-201367","type":"journal-article","created":{"date-parts":[[2021,1,22]],"date-time":"2021-01-22T16:02:23Z","timestamp":1611331343000},"page":"S195-S214","source":"Crossref","is-referenced-by-count":57,"title":["Gut Microbiota Alterations and Cognitive Impairment Are Sexually Dissociated in a Transgenic Mice Model of Alzheimer\u2019s Disease"],"prefix":"10.1177","volume":"82","author":[{"given":"Daniel","family":"Cuervo-Zanatta","sequence":"first","affiliation":[{"name":"Pharmacology Department, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Laboratory of Neuroplasticity and Neurodegeneration, Mexico City, Mexico"},{"name":"Genetics and Molecular Biology Department, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Laboratory of reference and support for the characterization of genomes, transcriptomes and microbiomes, Mexico City, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaime","family":"Garcia-Mena","sequence":"additional","affiliation":[{"name":"Genetics and Molecular Biology Department, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Laboratory of reference and support for the characterization of genomes, transcriptomes and microbiomes, Mexico City, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Perez-Cruz","sequence":"additional","affiliation":[{"name":"Pharmacology Department, Center for Research and Advanced Studies of the National Polytechnic Institute (Cinvestav), Laboratory of Neuroplasticity and Neurodegeneration, Mexico City, 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Sci"},{"key":"10.3233\/JAD-201367_ref8","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0162-3095(94)90020-5","article-title":"The hunter-gatherer theory of spatial sex differences: Proximate factors mediating the female advantage in recall of object arrays","volume":"15","author":"Eals","year":"1994","journal-title":"Ethol Sociobiol"},{"key":"10.3233\/JAD-201367_ref9","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/S1090-5138(97)00001-9","article-title":"Superior spatial memory of women: Stronger evidence for the gathering hypothesis","volume":"18","author":"McBurney","year":"1997","journal-title":"Evol Hum Behav"},{"key":"10.3233\/JAD-201367_ref10","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0191-8869(93)90174-2","article-title":"Sex differences in route-learning","volume":"14","author":"Galea","year":"1993","journal-title":"Pers Individ Dif"},{"key":"10.3233\/JAD-201367_ref11","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1037\/h0080690","article-title":"Individual differences in cognitive abilities and brain organization, part I: Sex and handedness differences in ability","volume":"37","author":"Harshman","year":"1983","journal-title":"Can J Psychol"},{"key":"10.3233\/JAD-201367_ref12","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1002\/ar.1092290311","article-title":"Effects of aging on the neuroglial cells and pericytes within area 17 of the rhesus monkey cerebral cortex","volume":"229","author":"Peters","year":"1991","journal-title":"Anat Rec"},{"key":"10.3233\/JAD-201367_ref13","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1037\/0033-2909.117.2.250","article-title":"Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables","volume":"117","author":"Voyer","year":"1995","journal-title":"Psychol Bull"},{"key":"10.3233\/JAD-201367_ref14","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1080\/13825580590925125","article-title":"Gender differences and cognition among older adults","volume":"12","author":"Parsons","year":"2005","journal-title":"Aging Neuropsychol Cogn"},{"key":"10.3233\/JAD-201367_ref15","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1093\/arclin\/7.5.407","article-title":"Rey auditory-verbal learning test: The effects of age and gender, and norms for delayed recall and story recognition trials","volume":"7","author":"Savage","year":"1992","journal-title":"Arch Clin Neuropsychol"},{"key":"10.3233\/JAD-201367_ref16","doi-asserted-by":"crossref","first-page":"54","DOI":"10.5498\/wjp.v6.i1.54","article-title":"Sex differences in cognitive impairment in Alzheimer\u2019s disease","volume":"6","author":"Laws","year":"2016","journal-title":"World J Psychiatry"},{"key":"10.3233\/JAD-201367_ref17","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1111\/j.1532-5415.1993.tb06738.x","article-title":"Effects of age, gender and education on selected neuropsychological tests in an elderly community cohort","volume":"41","author":"Wiederholt","year":"1993","journal-title":"J Am Geriatr Soc"},{"key":"10.3233\/JAD-201367_ref18","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s10508-006-9155-y","article-title":"Gender and sexual orientation differences in cognition across adulthood: Age is kinder to women than to men regardless of sexual orientation","volume":"36","author":"Maylor","year":"2007","journal-title":"Arch Sex Behav"},{"key":"10.3233\/JAD-201367_ref19","doi-asserted-by":"crossref","first-page":"P137","DOI":"10.1093\/geronb\/61.3.P137","article-title":"Sex differences after all those years? 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engender better detection of Alzheimer\u2019s disease in women","volume":"17","author":"Chapman","year":"2011","journal-title":"J Int Neuropsychol Soc"},{"key":"10.3233\/JAD-201367_ref26","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s00415-008-0726-9","article-title":"Gender-specificities in Alzheimer\u2019s disease and mild cognitive impairment","volume":"255","author":"Beinhoff","year":"2008","journal-title":"J Neurol"},{"key":"10.3233\/JAD-201367_ref27","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1001\/archneur.1996.00550050066025","article-title":"Gender comparisons of cognitive performances among vascular dementia, Alzheimer disease, and older adults without dementia","volume":"53","author":"Buckwalter","year":"1996","journal-title":"Arch Neurol"},{"key":"10.3233\/JAD-201367_ref28","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/s007370200011","article-title":"Gender differences in the cognitive impairment in Alzheimer\u2019s 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Protoc"},{"key":"10.3233\/JAD-201367_ref51","doi-asserted-by":"crossref","first-page":"e35538","DOI":"10.1371\/journal.pone.0035538","article-title":"Mouse estrous cycle identification tool and images","volume":"7","author":"Byers","year":"2012","journal-title":"PLoS One"},{"key":"10.3233\/JAD-201367_ref52","doi-asserted-by":"publisher","DOI":"10.1002\/0471142301.nsa04is48"},{"key":"10.3233\/JAD-201367_ref53","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1038\/nprot.2006.2","article-title":"T-maze alternation in the rodent","volume":"1","author":"Deacon","year":"2006","journal-title":"Nat Protoc"},{"key":"10.3233\/JAD-201367_ref54","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0166-4328(97)00214-3","article-title":"A new continuous alternation task in T-maze detects hippocampal dysfuncion in mice. A strain comparison and lesion study","volume":"95","author":"Gerlai","year":"1998","journal-title":"Behav Brain Res"},{"key":"10.3233\/JAD-201367_ref55","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.bbr.2017.05.005","article-title":"Water and T-maze protocols are equally efficient methods to assess spatial memory in 3xTg Alzheimer\u2019s disease mice","volume":"331","author":"Davis","year":"2017","journal-title":"Behav Brain Res"},{"key":"10.3233\/JAD-201367_ref56","doi-asserted-by":"crossref","first-page":"1657","DOI":"10.3233\/JAD-180556","article-title":"Bioactive food abates metabolic and synaptic alterations by modulation of the brain-gut axis in a mouse model of Alzheimer\u2019s disease","volume":"66","author":"Syeda","year":"2018","journal-title":"J Alzheimers Dis"},{"key":"10.3233\/JAD-201367_ref57","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.brainres.2012.05.041","article-title":"NMDA preconditioning prevents object recognition memory impairment and increases brain viability in mice exposed to traumatic brain injury","volume":"1466","author":"Moojen","year":"2012","journal-title":"Brain Res"},{"key":"10.3233\/JAD-201367_ref58","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.cortex.2017.05.016","article-title":"The role of the hippocampus in recognition memory","volume":"93","author":"Bird","year":"2017","journal-title":"Cortex"},{"key":"10.3233\/JAD-201367_ref59","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.bbr.2015.06.030","article-title":"Medial prefrontal cortex role in recognition memory in rodents","volume":"292","author":"Morici","year":"2015","journal-title":"Behav Brain Res"},{"key":"10.3233\/JAD-201367_ref60","doi-asserted-by":"publisher","DOI":"10.3791\/897"},{"key":"10.3233\/JAD-201367_ref61","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.lfs.2010.09.004","article-title":"Assessment of spatial memory in 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and lactic acid produced by intestinal bacteria during in vitro fermentation","volume":"80","author":"De Baere","year":"2013","journal-title":"J Pharm Biomed Anal"},{"key":"10.3233\/JAD-201367_ref65","doi-asserted-by":"crossref","first-page":"e9205","DOI":"10.7717\/peerj.9205","article-title":"Human milk microbiota associated with early colonization of the neonatal gut in Mexican newborns","volume":"8","author":"Corona-Cervantes","year":"2020","journal-title":"PeerJ"},{"key":"10.3233\/JAD-201367_ref66","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2004","journal-title":"Nat Methods"},{"key":"10.3233\/JAD-201367_ref67","doi-asserted-by":"crossref","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","article-title":"Metagenomic biomarker discovery and explanation","volume":"12","author":"Segata","year":"2011","journal-title":"Genome 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