{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,11]],"date-time":"2026-11-11T21:51:20Z","timestamp":1794433880045,"version":"4.9.1"},"reference-count":79,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T00:00:00Z","timestamp":1682553600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T00:00:00Z","timestamp":1682553600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["81801679"],"award-info":[{"award-number":["81801679"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["82071905"],"award-info":[{"award-number":["82071905"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Neurol"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>There is bidirectional communication between the gut microbiota and the brain. Empirical evidence has demonstrated sex differences in both the gut microbiome and the brain. However, the effects of sex on the gut microbiota-brain associations have yet to be determined. We aim to elucidate the sex-specific effects of gut microbiota on brain and cognition.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>One hundred fifty-seven healthy young adults underwent brain structural, perfusion, functional and diffusion MRIs to measure gray matter volume (GMV), cerebral blood flow (CBF), functional connectivity strength (FCS) and white matter integrity, respectively. Fecal samples were collected and 16S amplicon sequencing was utilized to assess gut microbial diversity. Correlation analyses were conducted to test for sex-dependent associations between microbial diversity and brain imaging parameters, and mediation analysis was performed to further characterize the gut microbiota-brain-cognition relationship.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We found that higher gut microbial diversity was associated with higher GMV in the right cerebellum VI, higher CBF in the bilateral calcarine sulcus yet lower CBF in the left superior frontal gyrus, higher FCS in the bilateral paracentral lobule, and lower diffusivity in widespread white matter regions in males. However, these associations were absent in females. Of more importance, these neuroimaging biomarkers significantly mediated the association between gut microbial diversity and behavioral inhibition in males.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>These findings highlight sex as a potential influential factor underlying the gut microbiota-brain-cognition relationship, and expose the gut microbiota as a biomarker-driven and sex-sensitive intervention target for mental disorders with abnormal behavioral inhibition.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12883-023-03217-3","type":"journal-article","created":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T05:02:54Z","timestamp":1682571774000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Sex-dependent gut microbiota-brain-cognition associations: a multimodal MRI study"],"prefix":"10.1186","volume":"23","author":[{"given":"Shujun","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huanhuan","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunli","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajia","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongqiang","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,4,27]]},"reference":[{"key":"3217_CR1","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1038\/s41392-022-00974-4","volume":"7","author":"K Hou","year":"2022","unstructured":"Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, et al. Microbiota in health and diseases. Signal Transduct Target Ther. 2022;7:135.","journal-title":"Signal Transduct Target Ther"},{"key":"3217_CR2","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1152\/physrev.00018.2018","volume":"99","author":"JF Cryan","year":"2019","unstructured":"Cryan JF, O\u2019Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99:1877\u20132013.","journal-title":"Physiol Rev"},{"key":"3217_CR3","first-page":"133","volume":"6","author":"CR Martin","year":"2018","unstructured":"Martin CR, Osadchiy V, Kalani A, Mayer EA. The brain-gut-microbiome axis, cell mol. Gastroenterol Hepatol. 2018;6:133\u201348.","journal-title":"Gastroenterol Hepatol"},{"key":"3217_CR4","doi-asserted-by":"publisher","first-page":"596","DOI":"10.3390\/biomedicines10030596","volume":"10","author":"MH Chiang","year":"2022","unstructured":"Chiang MH, Ho SM, Wu HY, Lin YC, Tsai WH, Wu T, et al. Drosophila model for studying gut microbiota in behaviors and neurodegenerative diseases. Biomedicines. 2022;10:596.","journal-title":"Biomedicines"},{"key":"3217_CR5","doi-asserted-by":"publisher","first-page":"2359","DOI":"10.1002\/jcp.25518","volume":"232","author":"R Mittal","year":"2017","unstructured":"Mittal R, Debs LH, Patel AP, Nguyen D, Patel K, O\u2019Connor G, et al. Neurotransmitters: the critical modulators regulating gut-brain axis. J Cell Physiol. 2017;232:2359\u201372.","journal-title":"J Cell Physiol"},{"key":"3217_CR6","doi-asserted-by":"publisher","first-page":"110468","DOI":"10.1016\/j.pnpbp.2021.110468","volume":"113","author":"J Zhu","year":"2022","unstructured":"Zhu J, Wang C, Qian Y, Cai H, Zhang S, Zhang C, et al. Multimodal neuroimaging fusion biomarkers mediate the association between gut microbiota and cognition. Prog Neuropsychopharmacol Biol Psychiatry. 2022;113:110468.","journal-title":"Prog Neuropsychopharmacol Biol Psychiatry"},{"key":"3217_CR7","doi-asserted-by":"publisher","first-page":"8171","DOI":"10.7150\/thno.35387","volume":"9","author":"YF Wang","year":"2019","unstructured":"Wang YF, Zheng LJ, Liu Y, Ye YB, Luo S, Lu GM, et al. The gut microbiota-inflammation-brain axis in end-stage renal disease: perspectives from default mode network. Theranostics. 2019;9:8171\u201381.","journal-title":"Theranostics"},{"key":"3217_CR8","doi-asserted-by":"publisher","first-page":"1821","DOI":"10.1007\/s00394-018-1732-z","volume":"58","author":"D Bagga","year":"2019","unstructured":"Bagga D, Aigner CS, Reichert JL, Cecchetto C, Fischmeister FPS, Holzer P, et al. Influence of 4-week multi-strain probiotic administration on resting-state functional connectivity in healthy volunteers. Eur J Nutr. 2019;58:1821\u20137.","journal-title":"Eur J Nutr"},{"key":"3217_CR9","doi-asserted-by":"publisher","first-page":"100815","DOI":"10.1016\/j.yfrne.2019.100815","volume":"56","author":"M Jaggar","year":"2020","unstructured":"Jaggar M, Rea K, Spichak S, Dinan TG, Cryan JF. You\u2019ve got male: Sex and the microbiota-gut-brain axis across the lifespan. Front Neuroendocrinol. 2020;56:100815.","journal-title":"Front Neuroendocrinol"},{"key":"3217_CR10","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1097\/MCG.0000000000001676","volume":"56","author":"M d\u2019Afflitto","year":"2022","unstructured":"d\u2019Afflitto M, Upadhyaya A, Green A, Peiris M. Association between sex hormone levels and gut microbiota composition and diversity\u2014a systematic review. J Clin Gastroenterol. 2022;56:384\u201392.","journal-title":"J Clin Gastroenterol"},{"key":"3217_CR11","doi-asserted-by":"publisher","first-page":"1917","DOI":"10.1111\/ejn.15666","volume":"55","author":"F Effah","year":"2022","unstructured":"Effah F, de Gusmao Taveiros Silva NK, Vijayanathan K, Camarini R, Joly F, Taiwo B, et al. Sex-dependent impact of microbiota status on cerebral mu-opioid receptor density in fischer rats. Eur J Neurosci. 2022;55:1917\u201333.","journal-title":"Eur J Neurosci"},{"key":"3217_CR12","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1186\/s12934-022-01783-8","volume":"21","author":"X Guo","year":"2022","unstructured":"Guo X, Sha Y, Lv W, Pu X, Liu X, Luo Y, et al. Sex differences in rumen fermentation and microbiota of Tibetan goat. Microb Cell Fact. 2022;21:55.","journal-title":"Microb Cell Fact"},{"key":"3217_CR13","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1186\/s40168-018-0587-0","volume":"6","author":"K Kaliannan","year":"2018","unstructured":"Kaliannan K, Robertson RC, Murphy K, Stanton C, Kang C, Wang B, et al. Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice. Microbiome. 2018;6:205.","journal-title":"Microbiome"},{"key":"3217_CR14","doi-asserted-by":"publisher","first-page":"e00017","DOI":"10.1128\/mSystems.00017-19","volume":"4","author":"J Zhang","year":"2019","unstructured":"Zhang J, Sun Z, Jiang S, Bai X, Ma C, Peng Q, et al. Probiotic bifidobacterium lactis V9 regulates the secretion of sex hormones in polycystic ovary syndrome patients through the Gut-Brain Axis. mSystems. 2019;4:e00017.","journal-title":"mSystems."},{"key":"3217_CR15","doi-asserted-by":"publisher","first-page":"2959","DOI":"10.1093\/cercor\/bhy109","volume":"28","author":"SJ Ritchie","year":"2018","unstructured":"Ritchie SJ, Cox SR, Shen X, Lombardo MV, Reus LM, Alloza C, et al. Sex differences in the adult human brain: evidence from 5216 UK biobank participants. Cereb Cortex. 2018;28:2959\u201375.","journal-title":"Cereb Cortex"},{"key":"3217_CR16","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1016\/j.biopsych.2007.03.001","volume":"62","author":"KP Cosgrove","year":"2007","unstructured":"Cosgrove KP, Mazure CM, Staley JK. Evolving knowledge of sex differences in brain structure, function, and chemistry. Biol Psychiatry. 2007;62:847\u201355.","journal-title":"Biol Psychiatry"},{"key":"3217_CR17","doi-asserted-by":"publisher","first-page":"407","DOI":"10.3389\/fcell.2020.00407","volume":"8","author":"GA Scott","year":"2020","unstructured":"Scott GA, Terstege DJ, Vu AP, Law S, Evans A, Epp JR. Disrupted neurogenesis in germ-free mice: effects of age and sex. Front Cell Dev Biol. 2020;8:407.","journal-title":"Front Cell Dev Biol"},{"key":"3217_CR18","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1186\/s13293-022-00422-6","volume":"13","author":"P Shobeiri","year":"2022","unstructured":"Shobeiri P, Kalantari A, Teixeira AL, Rezaei N. Shedding light on biological sex differences and microbiota-gut-brain axis: a comprehensive review of its roles in neuropsychiatric disorders. Biol Sex Differ. 2022;13:12.","journal-title":"Biol Sex Differ"},{"key":"3217_CR19","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1038\/nrgastro.2017.97","volume":"14","author":"MJ Claesson","year":"2017","unstructured":"Claesson MJ, Clooney AG, O\u2019Toole PW. A clinician\u2019s guide to microbiome analysis. Nat Rev Gastroenterol Hepatol. 2017;14:585\u201395.","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"3217_CR20","doi-asserted-by":"publisher","first-page":"50","DOI":"10.3389\/fnins.2020.00050","volume":"14","author":"Y Yang","year":"2020","unstructured":"Yang Y, Zhu DM, Zhang C, Zhang Y, Wang C, Zhang B, et al. Brain structural and functional alterations specific to low sleep efficiency in major depressive disorder. Front Neurosci. 2020;14:50.","journal-title":"Front Neurosci"},{"key":"3217_CR21","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1093\/schbul\/sbx051","volume":"43","author":"J Zhu","year":"2017","unstructured":"Zhu J, Zhuo C, Xu L, Liu F, Qin W, Yu C. altered coupling between resting-state cerebral blood flow and functional connectivity in schizophrenia. Schizophr Bull. 2017;43:1363\u201374.","journal-title":"Schizophr Bull"},{"key":"3217_CR22","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.jpsychires.2020.07.012","volume":"130","author":"C Zhang","year":"2020","unstructured":"Zhang C, Yang Y, Zhu DM, Zhao W, Zhang Y, Zhang B, et al. Neural correlates of the association between depression and high density lipoprotein cholesterol change. J Psychiatr Res. 2020;130:9\u201318.","journal-title":"J Psychiatr Res"},{"key":"3217_CR23","doi-asserted-by":"publisher","first-page":"7839","DOI":"10.1523\/JNEUROSCI.23-21-07839.2003","volume":"23","author":"JN Kaufman","year":"2003","unstructured":"Kaufman JN, Ross TJ, Stein EA, Garavan H. Cingulate hypoactivity in cocaine users during a GO-NOGO task as revealed by event-related functional magnetic resonance imaging. J Neurosci. 2003;23:7839\u201343.","journal-title":"J Neurosci"},{"key":"3217_CR24","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1037\/pha0000409","volume":"29","author":"A Venegas","year":"2021","unstructured":"Venegas A, Meredith LR, Green R, Cooper ZD, Ray LA. Sex-dependent effects of alcohol administration on the urge to use cannabis. Exp Clin Psychopharmacol. 2021;29:689\u201395.","journal-title":"Exp Clin Psychopharmacol"},{"key":"3217_CR25","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1002\/oby.22870","volume":"28","author":"TS Dong","year":"2020","unstructured":"Dong TS, Mayer EA, Osadchiy V, Chang C, Katzka W, Lagishetty V, et al. A distinct brain-gut-microbiome profile exists for females with obesity and food addiction. Obesity (Silver Spring). 2020;28:1477\u201386.","journal-title":"Obesity (Silver Spring)"},{"key":"3217_CR26","doi-asserted-by":"publisher","first-page":"102769","DOI":"10.1016\/j.ebiom.2020.102769","volume":"55","author":"VL Peterson","year":"2020","unstructured":"Peterson VL, Richards JB, Meyer PJ, Cabrera-Rubio R, Tripi JA, King CP, et al. Sex-dependent associations between addiction-related behaviors and the microbiome in outbred rats. EBioMedicine. 2020;55:102769.","journal-title":"EBioMedicine"},{"key":"3217_CR27","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1016\/j.neuroimage.2005.02.018","volume":"26","author":"J Ashburner","year":"2005","unstructured":"Ashburner J, Friston KJ. Unified segmentation. Neuroimage. 2005;26:839\u201351.","journal-title":"Neuroimage"},{"key":"3217_CR28","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/j.neuroimage.2007.07.007","volume":"38","author":"J Ashburner","year":"2007","unstructured":"Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. 2007;38:95\u2013113.","journal-title":"Neuroimage"},{"key":"3217_CR29","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1002\/mrm.1910400308","volume":"40","author":"RB Buxton","year":"1998","unstructured":"Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med. 1998;40:383\u201396.","journal-title":"Magn Reson Med"},{"key":"3217_CR30","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1192\/bjp.bp.115.174961","volume":"210","author":"C Zhuo","year":"2017","unstructured":"Zhuo C, Zhu J, Qin W, Qu H, Ma X, Yu C. Cerebral blood flow alterations specific to auditory verbal hallucinations in schizophrenia. Br J Psychiatry. 2017;210:209\u201315.","journal-title":"Br J Psychiatry"},{"key":"3217_CR31","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1002\/nbm.1462","volume":"23","author":"G Xu","year":"2010","unstructured":"Xu G, Rowley HA, Wu G, Alsop DC, Shankaranarayanan A, Dowling M, et al. Reliability and precision of pseudo-continuous arterial spin labeling perfusion MRI on 3.0 T and comparison with 15O-water PET in elderly subjects at risk for Alzheimer\u2019s disease. NMR Biomed. 2010;23:286\u201393.","journal-title":"NMR Biomed"},{"key":"3217_CR32","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.jpsychires.2015.03.002","volume":"63","author":"J Zhu","year":"2015","unstructured":"Zhu J, Zhuo C, Qin W, Xu Y, Xu L, Liu X, et al. Altered resting-state cerebral blood flow and its connectivity in schizophrenia. J Psychiatr Res. 2015;63:28\u201335.","journal-title":"J Psychiatr Res"},{"key":"3217_CR33","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1007\/s12021-016-9299-4","volume":"14","author":"CG Yan","year":"2016","unstructured":"Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics. 2016;14:339\u201351.","journal-title":"Neuroinformatics"},{"key":"3217_CR34","doi-asserted-by":"publisher","first-page":"9885","DOI":"10.1073\/pnas.1001414107","volume":"107","author":"D Tomasi","year":"2010","unstructured":"Tomasi D, Volkow ND. Functional connectivity density mapping. Proc Natl Acad Sci U S A. 2010;107:9885\u201390.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3217_CR35","doi-asserted-by":"publisher","first-page":"1862","DOI":"10.1093\/cercor\/bhr269","volume":"22","author":"XN Zuo","year":"2012","unstructured":"Zuo XN, Ehmke R, Mennes M, Imperati D, Castellanos FX, Sporns O, et al. Network centrality in the human functional connectome. Cereb Cortex. 2012;22:1862\u201375.","journal-title":"Cereb Cortex"},{"key":"3217_CR36","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1016\/j.pscychresns.2017.10.009","volume":"270","author":"J Zhu","year":"2017","unstructured":"Zhu J, Lin X, Lin C, Zhuo C. Distance-dependent alterations in local functional connectivity in drug-naive major depressive disorder. Psychiatry Res Neuroimaging. 2017;270:80\u20135.","journal-title":"Psychiatry Res Neuroimaging"},{"key":"3217_CR37","doi-asserted-by":"publisher","first-page":"1487","DOI":"10.1016\/j.neuroimage.2006.02.024","volume":"31","author":"SM Smith","year":"2006","unstructured":"Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006;31:1487\u2013505.","journal-title":"Neuroimage"},{"key":"3217_CR38","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/j.nicl.2014.12.008","volume":"7","author":"J Zhu","year":"2015","unstructured":"Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, et al. Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. Neuroimage Clin. 2015;7:170\u20136.","journal-title":"Neuroimage Clin"},{"key":"3217_CR39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/0006-3207(92)91201-3","volume":"61","author":"DP Faith","year":"1992","unstructured":"Faith DP. Conservation evaluation and phylogenetic diversity. Biol Conserv. 1992;61:1\u201310.","journal-title":"Biol Conserv"},{"key":"3217_CR40","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.0030-1299.2005.13735.x","volume":"109","author":"CJ Keylock","year":"2005","unstructured":"Keylock CJ. Simpson diversity and the Shannon-Wiener index as special cases of a generalized entropy. Oikos. 2005;109:203\u20137.","journal-title":"Oikos"},{"key":"3217_CR41","doi-asserted-by":"publisher","first-page":"7537","DOI":"10.1128\/AEM.01541-09","volume":"75","author":"PD Schloss","year":"2009","unstructured":"Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537\u201341.","journal-title":"Appl Environ Microbiol"},{"key":"3217_CR42","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/nmeth.f.303","volume":"7","author":"JG Caporaso","year":"2010","unstructured":"Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335\u20136.","journal-title":"Nat Methods"},{"key":"3217_CR43","first-page":"3698","volume":"27","author":"AD Nostro","year":"2017","unstructured":"Nostro AD, Muller VI, Reid AT, Eickhoff SB. Correlations between personality and brain structure: a crucial role of gender. Cereb Cortex. 2017;27:3698\u2013712.","journal-title":"Cereb Cortex"},{"key":"3217_CR44","unstructured":"Cohen J. The statistical power analysis for the behavioral sciences, 2nd ed. J Am Stat Assoc. 1988. p. 334."},{"key":"3217_CR45","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1080\/03637750903310360","volume":"76","author":"AF Hayes","year":"2009","unstructured":"Hayes AF. Beyond Baron and Kenny: statistical mediation analysis in the new millennium. Commun Monogr. 2009;76:408\u201320.","journal-title":"Commun Monogr"},{"key":"3217_CR46","first-page":"20150202","volume":"374","author":"IT Jolliffe","year":"2016","unstructured":"Jolliffe IT, Cadima J. Principal component analysis: a review and recent developments. Philos Trans A Math Phys Eng Sci. 2016;374:20150202.","journal-title":"Philos Trans A Math Phys Eng Sci"},{"key":"3217_CR47","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1097\/PSY.0000000000000493","volume":"79","author":"K Tillisch","year":"2017","unstructured":"Tillisch K, Mayer EA, Gupta A, Gill Z, Brazeilles R, Le Neve B, et al. Brain structure and response to emotional stimuli as related to gut microbial profiles in healthy women. Psychosom Med. 2017;79:905\u201313.","journal-title":"Psychosom Med"},{"key":"3217_CR48","doi-asserted-by":"publisher","first-page":"2446","DOI":"10.1111\/ejn.14305","volume":"50","author":"K Curtis","year":"2019","unstructured":"Curtis K, Stewart CJ, Robinson M, Molfese DL, Gosnell SN, Kosten TR, et al. Insular resting state functional connectivity is associated with gut microbiota diversity. Eur J Neurosci. 2019;50:2446\u201352.","journal-title":"Eur J Neurosci"},{"key":"3217_CR49","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1111\/cns.13451","volume":"27","author":"P Liu","year":"2021","unstructured":"Liu P, Jia XZ, Chen Y, Yu Y, Zhang K, Lin YJ, et al. Gut microbiota interacts with intrinsic brain activity of patients with amnestic mild cognitive impairment. CNS Neurosci Ther. 2021;27:163\u201373.","journal-title":"CNS Neurosci Ther"},{"key":"3217_CR50","doi-asserted-by":"publisher","first-page":"13426","DOI":"10.1038\/s41598-018-31695-w","volume":"8","author":"A Baars","year":"2018","unstructured":"Baars A, Oosting A, Lohuis M, Koehorst M, El Aidy S, Hugenholtz F, et al. Sex differences in lipid metabolism are affected by presence of the gut microbiota. Sci Rep. 2018;8:13426.","journal-title":"Sci Rep"},{"key":"3217_CR51","doi-asserted-by":"publisher","first-page":"e1800870","DOI":"10.1002\/mnfr.201800870","volume":"63","author":"JA Santos-Marcos","year":"2019","unstructured":"Santos-Marcos JA, Haro C, Vega-Rojas A, Alcala-Diaz JF, Molina-Abril H, Leon-Acuna A, et al. Sex differences in the gut microbiota as potential determinants of gender predisposition to disease. Mol Nutr Food Res. 2019;63:e1800870.","journal-title":"Mol Nutr Food Res"},{"key":"3217_CR52","doi-asserted-by":"publisher","first-page":"754","DOI":"10.3389\/fimmu.2017.00754","volume":"8","author":"F Fransen","year":"2017","unstructured":"Fransen F, van Beek AA, Borghuis T, Meijer B, Hugenholtz F, van der Gaast-de Jongh C, et al. The impact of gut microbiota on gender-specific differences in immunity. Front Immunol. 2017;8:754.","journal-title":"Front Immunol"},{"key":"3217_CR53","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1007\/s00281-018-0716-7","volume":"41","author":"R Vemuri","year":"2019","unstructured":"Vemuri R, Sylvia KE, Klein SL, Forster SC, Plebanski M, Eri R, et al. The microgenderome revealed: sex differences in bidirectional interactions between the microbiota, hormones, immunity and disease susceptibility. Semin Immunopathol. 2019;41:265\u201375.","journal-title":"Semin Immunopathol"},{"key":"3217_CR54","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1007\/s11682-017-9704-0","volume":"12","author":"C Zhuo","year":"2018","unstructured":"Zhuo C, Wang C, Wang L, Guo X, Xu Q, Liu Y, et al. Altered resting-state functional connectivity of the cerebellum in schizophrenia. Brain Imaging Behav. 2018;12:383\u20139.","journal-title":"Brain Imaging Behav"},{"key":"3217_CR55","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1007\/s12311-020-01165-z","volume":"19","author":"D Mannarelli","year":"2020","unstructured":"Mannarelli D, Pauletti C, Petritis A, Delle Chiaie R, Curra A, Trompetto C, et al. Effects of cerebellar tDCS on inhibitory control: evidence from a Go\/NoGo Task. Cerebellum. 2020;19:788.","journal-title":"Cerebellum."},{"key":"3217_CR56","doi-asserted-by":"publisher","first-page":"6670","DOI":"10.1038\/s41598-018-25190-5","volume":"8","author":"D Ma","year":"2018","unstructured":"Ma D, Wang AC, Parikh I, Green SJ, Hoffman JD, Chlipala G, et al. Ketogenic diet enhances neurovascular function with altered gut microbiome in young healthy mice. Sci Rep. 2018;8:6670.","journal-title":"Sci Rep"},{"key":"3217_CR57","doi-asserted-by":"publisher","first-page":"1368","DOI":"10.1177\/0271678X20918031","volume":"40","author":"S Tonomura","year":"2020","unstructured":"Tonomura S, Ihara M, Friedland RP. Microbiota in cerebrovascular disease: a key player and future therapeutic target. J Cereb Blood Flow Metab. 2020;40:1368\u201380.","journal-title":"J Cereb Blood Flow Metab"},{"key":"3217_CR58","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1038\/nature11087","volume":"485","author":"RD Bell","year":"2012","unstructured":"Bell RD, Winkler EA, Singh I, Sagare AP, Deane R, Wu Z, et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature. 2012;485:512\u20136.","journal-title":"Nature"},{"key":"3217_CR59","doi-asserted-by":"publisher","first-page":"263ra158","DOI":"10.1126\/scitranslmed.3009759","volume":"6","author":"V Braniste","year":"2014","unstructured":"Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6:263ra158.","journal-title":"Sci Transl Med"},{"key":"3217_CR60","doi-asserted-by":"publisher","first-page":"2434","DOI":"10.1161\/CIRCULATIONAHA.115.019645","volume":"133","author":"J Li","year":"2016","unstructured":"Li J, Lin S, Vanhoutte PM, Woo CW, Xu A. Akkermansia Muciniphila protects against atherosclerosis by preventing metabolic Endotoxemia-induced inflammation in Apoe-\/- Mice. Circulation. 2016;133:2434\u201346.","journal-title":"Circulation"},{"key":"3217_CR61","doi-asserted-by":"publisher","first-page":"392","DOI":"10.3389\/fncel.2015.00392","volume":"9","author":"JR Kelly","year":"2015","unstructured":"Kelly JR, Kennedy PJ, Cryan JF, Dinan TG, Clarke G, Hyland NP. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci. 2015;9:392.","journal-title":"Front Cell Neurosci"},{"key":"3217_CR62","doi-asserted-by":"publisher","first-page":"1162","DOI":"10.1523\/JNEUROSCI.1359-19.2019","volume":"40","author":"R Sadler","year":"2020","unstructured":"Sadler R, Cramer JV, Heindl S, Kostidis S, Betz D, Zuurbier KR, et al. Short-chain fatty acids improve Poststroke recovery via immunological mechanisms. J Neurosci. 2020;40:1162\u201373.","journal-title":"J Neurosci"},{"key":"3217_CR63","doi-asserted-by":"publisher","first-page":"8023","DOI":"10.1523\/JNEUROSCI.0789-07.2007","volume":"27","author":"C Urgesi","year":"2007","unstructured":"Urgesi C, Calvo-Merino B, Haggard P, Aglioti SM. Transcranial magnetic stimulation reveals two cortical pathways for visual body processing. J Neurosci. 2007;27:8023\u201330.","journal-title":"J Neurosci"},{"key":"3217_CR64","doi-asserted-by":"publisher","first-page":"17278","DOI":"10.1073\/pnas.2000523117","volume":"117","author":"B Li","year":"2020","unstructured":"Li B, Nguyen TP, Ma C, Dan Y. Inhibition of impulsive action by projection-defined prefrontal pyramidal neurons. Proc Natl Acad Sci U S A. 2020;117:17278\u201387.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"3217_CR65","doi-asserted-by":"publisher","first-page":"1641","DOI":"10.1007\/s00213-018-5161-8","volume":"236","author":"W Gao","year":"2019","unstructured":"Gao W, Salzwedel AP, Carlson AL, Xia K, Azcarate-Peril MA, Styner MA, et al. Gut microbiome and brain functional connectivity in infants-a preliminary study focusing on the amygdala. Psychopharmacology. 2019;236:1641\u201351.","journal-title":"Psychopharmacology"},{"key":"3217_CR66","doi-asserted-by":"crossref","unstructured":"Simpson S, Kimbrough A, Boomhower B, McLellan R, Hughes M, Shankar K, et al. Depletion of the microbiome alters the recruitment of neuronal ensembles of oxycodone intoxication and withdrawal. eNeuro. 2020;7:ENEURO.0312\u201319.2020.","DOI":"10.1523\/ENEURO.0312-19.2020"},{"key":"3217_CR67","doi-asserted-by":"publisher","first-page":"1394","DOI":"10.1053\/j.gastro.2013.02.043","volume":"144","author":"K Tillisch","year":"2013","unstructured":"Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J, Ebrat B, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology. 2013;144:1394\u20131401.e4.","journal-title":"Gastroenterology"},{"key":"3217_CR68","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1038\/s41398-017-0022-5","volume":"8","author":"IM Ong","year":"2018","unstructured":"Ong IM, Gonzalez JG, McIlwain SJ, Sawin EA, Schoen AJ, Adluru N, et al. Gut microbiome populations are associated with structure-specific changes in white matter architecture. Transl Psychiatry. 2018;8:6.","journal-title":"Transl Psychiatry"},{"key":"3217_CR69","doi-asserted-by":"publisher","first-page":"4505","DOI":"10.1210\/jc.2015-3076","volume":"100","author":"JM Fernandez-Real","year":"2015","unstructured":"Fernandez-Real JM, Serino M, Blasco G, Puig J, Daunis-i-Estadella J, Ricart W, et al. Gut microbiota interacts with brain microstructure and function. J Clin Endocrinol Metab. 2015;100:4505\u201313.","journal-title":"J Clin Endocrinol Metab"},{"key":"3217_CR70","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.mri.2019.02.006","volume":"58","author":"M Torres-Velazquez","year":"2019","unstructured":"Torres-Velazquez M, Sawin EA, Anderson JM, Yu JJ. Refractory diet-dependent changes in neural microstructure: Implications for microstructural endophenotypes of neurologic and psychiatric disease. Magn Reson Imaging. 2019;58:148\u201355.","journal-title":"Magn Reson Imaging"},{"key":"3217_CR71","doi-asserted-by":"publisher","unstructured":"Montoro RA, Singh AP, Yu JJ. Structural and functional neuroimaging of the effects of the gut microbiome. Eur Radiol. 2022:https:\/\/doi.org\/10.1007\/s00330-021-08486-5.","DOI":"10.1007\/s00330-021-08486-5"},{"key":"3217_CR72","doi-asserted-by":"publisher","first-page":"e774","DOI":"10.1038\/tp.2016.42","volume":"6","author":"AE Hoban","year":"2016","unstructured":"Hoban AE, Stilling RM, Ryan FJ, Shanahan F, Dinan TG, Claesson MJ, et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry. 2016;6:e774.","journal-title":"Transl Psychiatry"},{"key":"3217_CR73","doi-asserted-by":"publisher","first-page":"11960","DOI":"10.1523\/JNEUROSCI.3591-07.2007","volume":"27","author":"F Hoeft","year":"2007","unstructured":"Hoeft F, Barnea-Goraly N, Haas BW, Golarai G, Ng D, Mills D, et al. More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. J Neurosci. 2007;27:11960\u20135.","journal-title":"J Neurosci"},{"key":"3217_CR74","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1212\/WNL.0b013e3181d0ccdd","volume":"74","author":"AR Mayer","year":"2010","unstructured":"Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 2010;74:643\u201350.","journal-title":"Neurology"},{"key":"3217_CR75","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1016\/j.neuroimage.2009.09.046","volume":"49","author":"AV Witte","year":"2010","unstructured":"Witte AV, Savli M, Holik A, Kasper S, Lanzenberger R. Regional sex differences in grey matter volume are associated with sex hormones in the young adult human brain. Neuroimage. 2010;49:1205\u201312.","journal-title":"Neuroimage"},{"key":"3217_CR76","doi-asserted-by":"publisher","first-page":"e89095","DOI":"10.1371\/journal.pone.0089095","volume":"9","author":"NL Rasgon","year":"2014","unstructured":"Rasgon NL, Geist CL, Kenna HA, Wroolie TE, Williams KE, Silverman DH. Prospective randomized trial to assess effects of continuing hormone therapy on cerebral function in postmenopausal women at risk for dementia. PLoS ONE. 2014;9:e89095.","journal-title":"PLoS ONE"},{"key":"3217_CR77","doi-asserted-by":"publisher","unstructured":"Brugulat-Serrat A, Chen Y, Demnitz N, Ashour A, Adrion E, Ilinca S, et al. Roadmap for change in sex and gender inequities in brain health: a global perspective. Int J Geriatr Psychiatry. 2022;37:https:\/\/doi.org\/10.1002\/gps.5710.","DOI":"10.1002\/gps.5710"},{"key":"3217_CR78","doi-asserted-by":"publisher","first-page":"154","DOI":"10.1016\/j.neuroimage.2015.06.012","volume":"118","author":"N Lisofsky","year":"2015","unstructured":"Lisofsky N, Martensson J, Eckert A, Lindenberger U, Gallinat J, Kuhn S. Hippocampal volume and functional connectivity changes during the female menstrual cycle. Neuroimage. 2015;118:154\u201362.","journal-title":"Neuroimage"},{"key":"3217_CR79","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1186\/s12958-015-0107-z","volume":"13","author":"Z Liu","year":"2015","unstructured":"Liu Z, Liu J, Shi X, Wang L, Yang Y, Tao M. Dynamic alteration of serum testosterone with aging: a cross-sectional study from Shanghai. China, Reprod Biol Endocrinol. 2015;13:111.","journal-title":"China, Reprod Biol Endocrinol"}],"container-title":["BMC Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12883-023-03217-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12883-023-03217-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12883-023-03217-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,27]],"date-time":"2023-04-27T05:05:12Z","timestamp":1682571912000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcneurol.biomedcentral.com\/articles\/10.1186\/s12883-023-03217-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,27]]},"references-count":79,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["3217"],"URL":"https:\/\/doi.org\/10.1186\/s12883-023-03217-3","relation":{},"ISSN":["1471-2377"],"issn-type":[{"value":"1471-2377","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,27]]},"assertion":[{"value":"10 November 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 April 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 April 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Guidelines and regulations: This study was performed in accordance with the Declaration of Helsinki. Study approval statement: This study protocol was reviewed and approved by the Medical Ethics Committee of the First Affiliated Hospital of Anhui Medical University. Written informed consent was provided by all subjects.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"169"}}