{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,13]],"date-time":"2025-11-13T18:18:14Z","timestamp":1763057894477},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2015,8,6]],"date-time":"2015-08-06T00:00:00Z","timestamp":1438819200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2015,8,6]],"date-time":"2015-08-06T00:00:00Z","timestamp":1438819200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Inter-individual heterogeneity is evident in aging; education level is known to contribute for this heterogeneity. Using a cross-sectional study design and network inference applied to resting-state fMRI data, we show that aging was associated with decreased functional connectivity in a large cortical network. On the other hand, education level, as measured by years of formal education, produced an opposite effect on the long-term. These results demonstrate the increased brain efficiency in individuals with higher education level that may mitigate the impact of age on brain functional connectivity.<\/jats:p>","DOI":"10.1038\/srep12812","type":"journal-article","created":{"date-parts":[[2015,8,6]],"date-time":"2015-08-06T09:30:33Z","timestamp":1438853433000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":31,"title":["The Bounds Of Education In The Human Brain Connectome"],"prefix":"10.1038","volume":"5","author":[{"given":"P.","family":"Marques","sequence":"first","affiliation":[]},{"given":"J. M.","family":"Soares","sequence":"additional","affiliation":[]},{"given":"R.","family":"Magalh\u00e3es","sequence":"additional","affiliation":[]},{"given":"N. C.","family":"Santos","sequence":"additional","affiliation":[]},{"given":"N.","family":"Sousa","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2015,8,6]]},"reference":[{"key":"BFsrep12812_CR1","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1037\/0882-7974.18.3.510","volume":"18","author":"SW MacDonald","year":"2003","unstructured":"MacDonald, S. W., Hultsch, D. F. & Dixon, R. A. Performance variability is related to change in cognition: evidence from the Victoria Longitudinal Study. Psychology and aging 18, 510 (2003).","journal-title":"Psychology and aging"},{"key":"BFsrep12812_CR2","doi-asserted-by":"crossref","unstructured":"Santos, N. C. et al. Clinical, physical and lifestyle indicators and relationship with cognition and mood in aging: a cross-sectional analysis of distinct educational groups. Frontiers in Aging Neuroscience 6, 10.3389\/fnagi.2014.00021 (2014).","DOI":"10.3389\/fnagi.2014.00021"},{"key":"BFsrep12812_CR3","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1017\/S1355617702813248","volume":"8","author":"Y Stern","year":"2002","unstructured":"Stern, Y. What is cognitive reserve? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society: JINS 8, 448\u2013460 (2002).","journal-title":"Journal of the International Neuropsychological Society: JINS"},{"key":"BFsrep12812_CR4","doi-asserted-by":"publisher","first-page":"1114","DOI":"10.1016\/j.neurobiolaging.2007.10.008","volume":"30","author":"C Sole-Padulles","year":"2009","unstructured":"Sole-Padulles, C. et al. Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer\u2019s disease. Neurobiology of aging 30, 1114\u20131124, 10.1016\/j.neurobiolaging.2007.10.008 (2009).","journal-title":"Neurobiology of aging"},{"key":"BFsrep12812_CR5","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1038\/nrn2575","volume":"10","author":"E Bullmore","year":"2009","unstructured":"Bullmore, E. & Sporns, O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nature reviews. Neuroscience 10, 186\u2013198, 10.1038\/nrn2575 (2009).","journal-title":"Nature reviews. Neuroscience"},{"key":"BFsrep12812_CR6","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.mri.2010.06.027","volume":"29","author":"A Zalesky","year":"2011","unstructured":"Zalesky, A. Moderating registration misalignment in voxelwise comparisons of DTI data: a performance evaluation of skeleton projection. Magnetic resonance imaging 29, 111\u2013125, 10.1016\/j.mri.2010.06.027 (2011).","journal-title":"Magnetic resonance imaging"},{"key":"BFsrep12812_CR7","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1016\/j.biopsych.2011.05.018","volume":"70","author":"J Zhang","year":"2011","unstructured":"Zhang, J. et al. Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biological psychiatry 70, 334\u2013342, 10.1016\/j.biopsych.2011.05.018 (2011).","journal-title":"Biological psychiatry"},{"key":"BFsrep12812_CR8","doi-asserted-by":"publisher","first-page":"2186","DOI":"10.1162\/jocn_a_00269","volume":"24","author":"K Onoda","year":"2012","unstructured":"Onoda, K., Ishihara, M. & Yamaguchi, S. Decreased functional connectivity by aging is associated with cognitive decline. Journal of cognitive neuroscience 24, 2186\u20132198, 10.1162\/jocn_a_00269 (2012).","journal-title":"Journal of cognitive neuroscience"},{"key":"BFsrep12812_CR9","doi-asserted-by":"publisher","first-page":"2193","DOI":"10.1016\/j.neurobiolaging.2014.04.007","volume":"35","author":"R Sala-Llonch","year":"2014","unstructured":"Sala-Llonch, R. et al. Changes in whole-brain functional networks and memory performance in aging. Neurobiology of aging 35, 2193\u20132202, 10.1016\/j.neurobiolaging.2014.04.007 (2014).","journal-title":"Neurobiology of aging"},{"key":"BFsrep12812_CR10","doi-asserted-by":"publisher","first-page":"e17","DOI":"10.1371\/journal.pcbi.0030017","volume":"3","author":"S Achard","year":"2007","unstructured":"Achard, S. & Bullmore, E. Efficiency and cost of economical brain functional networks. PLoS computational biology 3, e17, 10.1371\/journal.pcbi.0030017 (2007).","journal-title":"PLoS computational biology"},{"key":"BFsrep12812_CR11","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1016\/j.neuroimage.2008.09.062","volume":"44","author":"D Meunier","year":"2009","unstructured":"Meunier, D., Achard, S., Morcom, A. & Bullmore, E. Age-related changes in modular organization of human brain functional networks. Neuroimage 44, 715\u2013723, 10.1016\/j.neuroimage.2008.09.062 (2009).","journal-title":"Neuroimage"},{"key":"BFsrep12812_CR12","doi-asserted-by":"publisher","first-page":"1425","DOI":"10.1016\/j.neuroimage.2009.05.015","volume":"47","author":"W van der Zwaag","year":"2009","unstructured":"van der Zwaag, W. et al. fMRI at 1.5, 3 and 7 T: characterising BOLD signal changes. Neuroimage 47, 1425\u20131434, 10.1016\/j.neuroimage.2009.05.015 (2009).","journal-title":"Neuroimage"},{"key":"BFsrep12812_CR13","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1212\/WNL.57.4.632","volume":"57","author":"M O\u2019Sullivan","year":"2001","unstructured":"O\u2019Sullivan, M. et al. Evidence for cortical \u201cdisconnection\u201d as a mechanism of age-related cognitive decline. Neurology 57, 632\u2013638 (2001).","journal-title":"Neurology"},{"key":"BFsrep12812_CR14","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1093\/brain\/122.5.963","volume":"122","author":"G Esposito","year":"1999","unstructured":"Esposito, G., Kirkby, B. S., Van Horn, J. D., Ellmore, T. M. & Berman, K. F. Context-dependent, neural system-specific neurophysiological concomitants of ageing: mapping PET correlates during cognitive activation. Brain: a journal of neurology 122 (Pt 5), 963\u2013979 (1999).","journal-title":"Brain: a journal of neurology"},{"key":"BFsrep12812_CR15","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1017\/s1355617709990385","volume":"15","author":"TA Salthouse","year":"2009","unstructured":"Salthouse, T. A. Decomposing age correlations on neuropsychological and cognitive variables. Journal of the International Neuropsychological Society: JINS 15, 650\u2013661, 10.1017\/s1355617709990385 (2009).","journal-title":"Journal of the International Neuropsychological Society: JINS"},{"key":"BFsrep12812_CR16","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/S0301-0511(00)00052-1","volume":"54","author":"TA Salthouse","year":"2000","unstructured":"Salthouse, T. A. Aging and measures of processing speed. Biological psychology 54, 35\u201354 (2000).","journal-title":"Biological psychology"},{"key":"BFsrep12812_CR17","doi-asserted-by":"publisher","first-page":"1201","DOI":"10.1093\/cercor\/bhm155","volume":"18","author":"SW Davis","year":"2008","unstructured":"Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S. & Cabeza, R. Que PASA? The posterior-anterior shift in aging. Cerebral cortex (New York, N.Y.: 1991) 18, 1201\u20131209, 10.1093\/cercor\/bhm155 (2008).","journal-title":"Cerebral cortex"},{"key":"BFsrep12812_CR18","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1016\/j.neuroimage.2009.01.068","volume":"46","author":"SW Davis","year":"2009","unstructured":"Davis, S. W. et al. Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 46, 530\u2013541 (2009).","journal-title":"Neuroimage"},{"key":"BFsrep12812_CR19","doi-asserted-by":"publisher","first-page":"1723","DOI":"10.1016\/j.neuroimage.2003.07.032","volume":"20","author":"C Habeck","year":"2003","unstructured":"Habeck, C. et al. Relation of cognitive reserve and task performance to expression of regional covariance networks in an event-related fMRI study of nonverbal memory. Neuroimage 20, 1723\u20131733 (2003).","journal-title":"Neuroimage"},{"key":"BFsrep12812_CR20","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1037\/a0014012","volume":"45","author":"EM Tucker-Drob","year":"2009","unstructured":"Tucker-Drob, E. M., Johnson, K. E. & Jones, R. N. The cognitive reserve hypothesis: a longitudinal examination of age-associated declines in reasoning and processing speed. Developmental psychology 45, 431\u2013446, 10.1037\/a0014012 (2009).","journal-title":"Developmental psychology"},{"key":"BFsrep12812_CR21","doi-asserted-by":"publisher","first-page":"243","DOI":"10.3233\/JAD-141824","volume":"44","author":"M Bozzali","year":"2015","unstructured":"Bozzali, M. et al. The impact of cognitive reserve on brain functional connectivity in Alzheimer\u2019s disease. Journal of Alzheimer\u2019s disease: JAD 44, 243\u2013250, 10.3233\/JAD-141824 (2015).","journal-title":"Journal of Alzheimer\u2019s disease: JAD"},{"key":"BFsrep12812_CR22","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1093\/brain\/121.4.561","volume":"121","author":"JD Schmahmann","year":"1998","unstructured":"Schmahmann, J. D. & Sherman, J. C. The cerebellar cognitive affective syndrome. Brain: a journal of neurology 121 (Pt 4), 561\u2013579 (1998).","journal-title":"Brain: a journal of neurology"},{"key":"BFsrep12812_CR23","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1007\/s11065-010-9142-x","volume":"20","author":"JD Schmahmann","year":"2010","unstructured":"Schmahmann, J. D. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis and its historical evolution from theory to therapy. Neuropsychology review 20, 236\u2013260, 10.1007\/s11065-010-9142-x (2010).","journal-title":"Neuropsychology review"},{"key":"BFsrep12812_CR24","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1093\/brain\/awh729","volume":"129","author":"JD Schmahmann","year":"2006","unstructured":"Schmahmann, J. D. & Caplan, D. Cognition, emotion and the cerebellum. Brain: a journal of neurology 129, 290\u2013292, 10.1093\/brain\/awh729 (2006).","journal-title":"Brain: a journal of neurology"},{"key":"BFsrep12812_CR25","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1002\/hbm.20575","volume":"30","author":"MC Bonnet","year":"2009","unstructured":"Bonnet, M. C. et al. Differential cerebellar and cortical involvement according to various attentional load: role of educational level. Human brain mapping 30, 1133\u20131143, 10.1002\/hbm.20575 (2009).","journal-title":"Human brain mapping"},{"key":"BFsrep12812_CR26","first-page":"9","volume":"1","author":"M Guerreiro","year":"1994","unstructured":"Guerreiro, M. et al. Adapta\u00e7\u00e3o \u00e0 popula\u00e7\u00e3o portuguesa da tradu\u00e7\u00e3o do Mini Mental State Examination (MMSE). Revista Portuguesa de Neurologia 1, 9\u201310 (1994).","journal-title":"Neurologia"},{"key":"BFsrep12812_CR27","doi-asserted-by":"publisher","first-page":"1983","DOI":"10.1007\/s11357-012-9482-y","volume":"35","author":"NC Santos","year":"2013","unstructured":"Santos, N. C. et al. Mood is a key determinant of cognitive performance in community-dwelling older adults: a cross-sectional analysis. Age (Dordrecht, Netherlands) 35, 1983\u20131993, 10.1007\/s11357-012-9482-y (2013).","journal-title":"Age (Dordrecht, Netherlands)"},{"key":"BFsrep12812_CR28","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1006\/nimg.2001.0978","volume":"15","author":"N Tzourio-Mazoyer","year":"2002","unstructured":"Tzourio-Mazoyer, N. et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273\u2013289, 10.1006\/nimg.2001.0978 (2002).","journal-title":"Neuroimage"},{"key":"BFsrep12812_CR29","doi-asserted-by":"publisher","first-page":"1271","DOI":"10.1016\/j.neurobiolaging.2005.05.016","volume":"26","author":"TL Jernigan","year":"2005","unstructured":"Jernigan, T. L. & Gamst, A. C. Changes in volume with age\u2013consistency and interpretation of observed effects. Neurobiology of aging 26, 1271\u20131274; discussion 1275-1278, 10.1016\/j.neurobiolaging.2005.05.016 (2005).","journal-title":"Neurobiology of aging"},{"key":"BFsrep12812_CR30","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1016\/j.neuroimage.2010.06.041","volume":"53","author":"A Zalesky","year":"2010","unstructured":"Zalesky, A., Fornito, A. & Bullmore, E. T. Network-based statistic: identifying differences in brain networks. Neuroimage 53, 1197\u20131207, 10.1016\/j.neuroimage.2010.06.041 (2010).","journal-title":"Neuroimage"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep12812","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep12812.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep12812.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T21:50:49Z","timestamp":1672955449000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep12812"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,8,6]]},"references-count":30,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2015,10,16]]}},"alternative-id":["BFsrep12812"],"URL":"https:\/\/doi.org\/10.1038\/srep12812","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,8,6]]},"assertion":[{"value":"18 March 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 July 2015","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 August 2015","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"12812"}}