Abstract
We evaluated the correlation of educational attainment with structural volume and shape morphometry of the bilateral hippocampi and amygdalae in a sample of 110 non-demented, older adults at elevated sociodemographic risk for cognitive and functional declines. In both men and women, no significant education–volume correlation was detected for either structure. However, when performing shape analysis, we observed regionally specific associations with education after adjusting for age, intracranial volume, and race. By sub-dividing the hippocampus and the amygdala into compatible subregions, we found that education was positively associated with size variations in the CA1 and subiculum subregions of the hippocampus and the basolateral subregion of the amygdala (p < 0.05). In addition, we detected a greater left versus right asymmetric pattern in the shape-education correlation for the hippocampus but not the amygdala. This asymmetric association was largely observed in men versus women. These findings suggest that education in youth may exert direct and indirect influences on brain reserve in regions that are most vulnerable to the neuropathologies of aging, dementia, and specifically, Alzheimer disease.
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References
Ali AE, Wilson YM, Murphy M (2009) A single exposure to an enriched environment stimulates the activation of discrete neuronal populations in the brain of the fos-tau-lacZ mouse. Neurobiol Learn Mem 92:381–390. doi:10.1016/j.nlm.2009.05.004
Austad SN (2006) Why women live longer than men: sex differences in longevity. Gend Med 3:79–92. doi:10.1016/S1550-8579(06)80198-1
Barulli D, Stern Y (2013) Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci (Regul Ed) 17:502–509. doi:10.1016/j.tics.2013.08.012
Basso M, Yang J, Warren L, MacAvoy MG, Varma P, Bronen RA, van Dyck CH (2006) Volumetry of amygdala and hippocampus and memory performance in Alzheimer’s disease. Psychiatry Res 146:251–261. doi:10.1016/j.pscychresns.2006.01.007
Beg MF, Miller MI, Trouvé A, Younes L (2005) Computing large deformation metric mappings via geodesic flows of diffeomorphisms. Int J Comput Vision 61:139–157. doi:10.1023/B:VISI.0000043755.93987.aa
Bennett DA, Wilson RS, Schneider JA, Evans DA, Mendes de Leon CF, Arnold SE, Barnes LL, Bienias JL (2003) Education modifies the relation of AD pathology to level of cognitive function in older persons. Neurology 60:1909–1915. doi:10.1212/01.WNL.0000069923.64550.9F
Braak H, Braak E (1995) Staging of Alzheimer’s disease-related neurofibrillary changes. Neurobiol Aging 16:271–278 (discussion 278-84; pii 0197458095000216)
Bruandet A, Richard F, Bombois S, Maurage CA, Masse I, Amouyel P, Pasquier F (2008) Cognitive decline and survival in Alzheimer’s disease according to education level. Dement Geriatr Cogn Disord 25:74–80 (pii 000111693)
Buckner RL, Head D, Parker J, Fotenos AF, Marcus D, Morris JC, Snyder AZ (2004) A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23:724–738. doi:10.1016/j.neuroimage.2004.06.018
Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641
Carlson MC, Saczynski JS, Rebok GW, Seeman T, Glass TA, McGill S, Tielsch J, Frick KD, Hill J, Fried LP (2008) Exploring the effects of an “Everyday” activity program on executive function and memory in older adults: experience corps®. Gerontologist 48:793–801. doi:10.1093/geront/48.6.793
Carlson MC, Erickson KI, Kramer AF, Voss MW, Bolea N, Mielke M, McGill S, Rebok GW, Seeman T, Fried LP (2009) Evidence for neurocognitive plasticity in at-risk older adults: the experience corps program. J Gerontol A Biol Sci Med Sci 64:1275–1282. doi:10.1093/gerona/glp117
Carlson MC, Seplaki CL, Seeman TE (2012) Reversing the impact of disparities in socioeconomic status over the life course on cognitive and brain aging. In: Wolfe B, Evans WN, Seeman TE (eds) The biological consequences of socioeconomic inequalities. Russell Sage Foundation Publications, New York, pp 215–247
Carlson MC, Kuo JH, Chuang Y, Varma VR, Harris G, Albert MS, Erickson KI, Kramer AF, Parisi JM, Xue Q et al (2015) Impact of the Baltimore Experience Corps Trial on cortical and hippocampal volumes. Alzheimer’s Dement. doi:10.1016/j.jalz.2014.12.005
Carmichael O, Xie J, Fletcher E, Singh B, DeCarli C, Alzheimer’s Disease Neuroimaging Initiative (2012) Localized hippocampus measures are associated with Alzheimer pathology and cognition independent of total hippocampal volume. Neurobiol Aging 33:1124.e31-1124.e41. doi: 10.1016/j.neurobiolaging.2011.08.016
Cavedo E, Galluzzi S, Pievani M, Boccardi M, Frisoni GB (2012) Norms for imaging markers of brain reserve. J Alzheimers Dis 31:623–633. doi:10.3233/JAD-2012-111817
Chelune GJ (1995) Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 10:413–432. doi:10.1093/arclin/10.5.413
Cherbuin N, Mortby ME, Janke AL, Sachdev PS, Abhayaratna WP, Anstey KJ (2015) Blood pressure, brain structure, and cognition: opposite associations in men and women. Am J Hypertens 28:225–231. doi:10.1093/ajh/hpu120
Chou YY, Lepore N, Avedissian C, Madsen SK, Parikshak N, Hua X, Shaw LM, Trojanowski JQ, Weiner MW, Toga AW et al (2009) Mapping correlations between ventricular expansion and CSF amyloid and tau biomarkers in 240 subjects with Alzheimer’s disease, mild cognitive impairment and elderly controls. Neuroimage 46:394–410. doi:10.1016/j.neuroimage.2009.02.015
Chuang Y, Eldreth D, Erickson KI, Varma V, Harris G, Fried LP, Rebok GW, Tanner EK, Carlson MC (2014) Cardiovascular risks and brain function: a functional magnetic resonance imaging study of executive function in older adults. Neurobiol Aging 35:1396–1403. doi:10.1016/j.neurobiolaging.2013.12.008
Cuénod C, Denys A, Michot J, Jehenson P, Forette F, Kaplan D, Syrota A, Boller F (1993) Amygdala atrophy in Alzheimer’s disease: an in vivo magnetic resonance imaging study. Arch Neurol 50:941–945
de Toledo-Morrell L, Dickerson B, Sullivan MP, Spanovic C, Wilson R, Bennett DA (2000) Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer’s disease. Hippocampus 10:136–142. doi:10.1002/(SICI)1098-1063(2000)10:23.0.CO;2-J
Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302
Draganski B, Gaser C, Kempermann G, Kuhn HG, Winkler J, Büchel C, May A (2006) Temporal and spatial dynamics of brain structure changes during extensive learning. J Neurosci 26:6314–6317. doi:10.1523/JNEUROSCI.4628-05.2006
Erten-Lyons D, Woltjer RL, Dodge H, Nixon R, Vorobik R, Calvert JF, Leahy M, Montine T, Kaye J (2009) Factors associated with resistance to dementia despite high Alzheimer disease pathology. Neurology 72:354–360. doi:10.1212/01.wnl.0000341273.18141.64
Evans DA, Beckett LA, Albert MS, Hebert LE, Scherr PA, Funkenstein HH, Taylor JO (1993) Level of education and change in cognitive function in a community population of older persons. Ann Epidemiol 3:71–77. doi:10.1016/1047-2797(93)90012-S
Farmer ME, Kittner SJ, Rae DS, Bartko JJ, Regier DA (1995) Education and change in cognitive function: the epidemiologic catchment area study. Ann Epidemiol 5:1–7. doi:10.1016/1047-2797(94)00047-W
Fortin NJ, Agster KL, Eichenbaum HB (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458–462
Fried LP, Carlson MC, McGill S, Seeman T, Xue Q, Frick K, Tan E, Tanner EK, Barron J, Frangakis C et al (2013) Experience Corps: a dual trial to promote the health of older adults and children’s academic success. Contemp Clin Trials 36:1–13. doi:10.1016/j.cct.2013.05.003
Fritsch T, McClendon MJ, Smyth KA, Ogrocki PK (2002) Effects of educational attainment and occupational status on cognitive and functional decline in persons with Alzheimer-type dementia. Int Psychogeriatr 14:347–363
Garibotto V, Borroni B, Sorbi S, Cappa SF, Padovani A, Perani D (2012) Education and occupation provide reserve in both ApoE ε4 carrier and noncarrier patients with probable Alzheimer’s disease. Neurol Sci 33:1037–1042. doi:10.1007/s10072-011-0889-5
Graves AB, Mortimer JA, Larson EB, Wenzlow A, Bowen JD, McCormick WC (1996) Head circumference as a measure of cognitive reserve. Association with severity of impairment in Alzheimer’s disease. Br J Psychiatry 169:86–92
Groppe DM, Urbach TP, Kutas M (2011) Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. Psychophysiology 48:1711–1725. doi:10.1111/j.1469-8986.2011.01273.x
Gur RC, Mozley PD, Resnick SM, Gottlieb GL, Kohn M, Zimmerman R, Herman G, Atlas S, Grossman R, Berretta D (1991) Gender differences in age effect on brain atrophy measured by magnetic resonance imaging. Proc Natl Acad Sci 88:2845–2849. doi:10.1073/pnas.88.7.2845
Hall CB, Derby C, LeValley A, Katz MJ, Verghese J, Lipton RB (2007) Education delays accelerated decline on a memory test in persons who develop dementia. Neurology 69:1657–1664 (pii 69/17/1657)
Horinek D, Varjassyova A, Hort J (2007) Magnetic resonance analysis of amygdalar volume in Alzheimer’s disease. Curr Opin Psychiatry 20:273–277. doi:10.1097/YCO.0b013e3280ebb613
Jenkins R, Fox NC, Rossor AM, Harvey RJ, Rossor MN (2000) Intracranial volume and Alzheimer disease: evidence against the cerebral reserve hypothesis. Arch Neurol 57:220–224
Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–495
LeDoux JE (1993) Emotional memory systems in the brain. Behav Brain Res 58:69–79
Lessov-Schlaggar CN, Reed T, Swan GE, Krasnow RE, DeCarli C, Marcus R, Holloway L, Wolf PA, Carmelli D (2005) Association of sex steroid hormones with brain morphology and cognition in healthy elderly men. Neurology 65:1591–1596 (pii 65/10/1591)
Letenneur L, Gilleron V, Commenges D, Helmer C, Orgogozo JM, Dartigues JF (1999) Are sex and educational level independent predictors of dementia and Alzheimer’s disease? Incidence data from the PAQUID project. J Neurol Neurosurg Psychiatry 66:177–183
Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neuropsychological assessment, 5th edn. Oxford University Press, New York
Locascio JJ, Growdon JH, Corkin S (1995) Cognitive test performance in detecting, staging, and tracking Alzheimer’s disease. Arch Neurol 52:1087–1099
Ma J, Miller MI, Younes L (2010) A bayesian generative model for surface template estimation. Int J Biomed Imaging 2010:974957. doi:10.1155/2010/974957 (Epub 20 Sep 2010)
Manly JJ, Jacobs DM, Touradji P, Small SA, Stern Y (2002) Reading level attenuates differences in neuropsychological test performance between African American and White elders. J Int Neuropsychol Soc 8:341–348
Manly JJ, Touradji P, Tang MX, Stern Y (2003) Literacy and memory decline among ethnically diverse elders. J Clin Exp Neuropsychol 25:680–690. doi:10.1076/jcen.25.5.680.14579
McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 107:3
McEwen BS, Gianaros PJ (2010) Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. Ann N Y Acad Sci 1186:190–222. doi:10.1111/j.1749-6632.2009.05331.x
McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28
Mielke MM, Vemuri P, Rocca WA (2014) Clinical epidemiology of Alzheimer’s disease: assessing sex and gender differences. Clin Epidemiol 6:37–48. doi:10.2147/CLEP.S37929
Miller MI, Younes L, Ratnanather JT, Brown T, Trinh H, Lee DS, Tward D, Mahon PB, Mori S, Albert M (2015) Amygdalar atrophy in symptomatic Alzheimer’s disease based on diffeomorphometry: the BIOCARD cohort. Neurobiol Aging 36(Supplement 1):S3–S10. doi:10.1016/j.neurobiolaging.2014.06.032
Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus
Mortimer JA, Snowdon DA, Markesbery WR (2003) Head circumference, education and risk of dementia: findings from the Nun Study. J Clin Exp Neuropsychol 25:671–679
Müller MJ, Greverus D, Dellani PR, Weibrich C, Wille PR, Scheurich A, Stoeter P, Fellgiebel A (2005) Functional implications of hippocampal volume and diffusivity in mild cognitive impairment. Neuroimage 28:1033–1042. doi:10.1016/j.neuroimage.2005.06.029
Murphy DM, DeCarli C, Mclntosh AR et al (1996) Sex differences in human brain morphometry and metabolism: an in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. Arch Gen Psychiatry 53:585–594. doi:10.1001/archpsyc.1996.01830070031007
Nichols T, Hayasaka S (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 12:419–446. doi:10.1191/0962280203sm341ra
Nordahl H, Lange T, Osler M, Diderichsen F, Andersen I, Prescott E, Tjonneland A, Frederiksen BL, Rod NH (2014) Education and cause-specific mortality: the mediating role of differential exposure and vulnerability to behavioral risk factors. Epidemiology 25:389–396. doi:10.1097/EDE.0000000000000080
Oksuzyan A, Juel K, Vaupel JW, Christensen K (2008) Men: good health and high mortality. Sex differences in health and aging. Aging Clin Exp Res 20:91–102 (pii 4534)
Parisi JM, Kuo J, Rebok GW, Xue Q, Fried LP, Gruenewald TL, Huang J, Seeman TE, Roth DL, Tanner EK (2015) Increases in lifestyle activities as a result of Experience Corps® Participation. J Urban Health 92:55–66
Perneczky R, Drzezga A, Diehl-Schmid J, Li Y, Kurz A (2007) Gender differences in brain reserve. J Neurol 254:1395–1400. doi:10.1007/s00415-007-0558-z
Perneczky R, Wagenpfeil S, Lunetta KL, Cupples LA, Green RC, Decarli C, Farrer LA, Kurz A, MIRAGE Study Group (2010) Head circumference, atrophy, and cognition: implications for brain reserve in Alzheimer disease. Neurology 75:137–142. doi:10.1212/WNL.0b013e3181e7ca97
Phelps EA (2004) Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14:198–202
Piras F, Cherubini A, Caltagirone C, Spalletta G (2011) Education mediates microstructural changes in bilateral hippocampus. Hum Brain Mapp 32:282–289. doi:10.1002/hbm.21018
Qiu A, Brown T, Fischl B, Ma J, Miller MI (2010) Atlas generation for subcortical and ventricular structures with its applications in shape analysis. Image Process IEEE Trans 19:1539–1547. doi:10.1109/TIP.2010.2042099
Rey A (1941) L’examen psychologique dans les cas d’encéphalopathie traumatique. (Les problems.). [The psychological examination in cases of traumatic encepholopathy. Problems.]. Arch Psychol 28:215–285
Richards M, Sacker A (2003) Lifetime antecedents of cognitive reserve. J Clin Exp Neuropsychol 25:614–624. doi:10.1076/jcen.25.5.614.14581
Roe CM, Xiong C, Miller JP, Morris JC (2007) Education and Alzheimer disease without dementia: support for the cognitive reserve hypothesis. Neurology 68:223–228 (pii 68/3/223)
Rossler M, Zarski R, Bohl J, Ohm TG (2002) Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer’s disease. Acta Neuropathol 103:363–369. doi:10.1007/s00401-001-0475-7
Sattler C, Toro P, Schonknecht P, Schroder J (2012) Cognitive activity, education and socioeconomic status as preventive factors for mild cognitive impairment and Alzheimer’s disease. Psychiatry Res 196:90–95. doi:10.1016/j.psychres.2011.11.012
Satz P (1993) Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology 7:273
Scarmeas N, Stern Y (2003) Cognitive reserve and lifestyle. J Clin Exp Neuropsychol 25:625–633. doi:10.1076/jcen.25.5.625.14576
Schmand B, Smit J, Lindeboom J, Smits C, Hooijer C, Jonker C, Deelman B (1997) Low education is a genuine risk factor for accelerated memory decline and dementia. J Clin Epidemiol 50:1025–1033. doi:10.1016/S0895-4356(97)00121-2
Schofield PW, Logroscino G, Andrews HF, Albert S, Stern Y (1997) An association between head circumference and Alzheimer’s disease in a population-based study of aging and dementia. Neurology 49:30–37
Schonheit B, Zarski R, Ohm TG (2004) Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging 25:697–711. doi:10.1016/j.neurobiolaging.2003.09.009
Soininen HS, Partanen K, Pitkanen A, Vainio P, Hanninen T, Hallikainen M, Koivisto K, Riekkinen PJS (1994) Volumetric MRI analysis of the amygdala and the hippocampus in subjects with age-associated memory impairment: correlation to visual and verbal memory. Neurology 44:1660–1668
Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195
Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 8:448–460
Stern Y (2009) Cognitive reserve. Neuropsychologia 47:2015–2028. doi:10.1016/j.neuropsychologia.2009.03.004
Stern Y (2012) Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol 11:1006–1012. doi:10.1016/S1474-4422(12)70191-6
Stern Y, Alexander GE, Prohovnik I, Mayeux R (1992) Inverse relationship between education and parietotemporal perfusion deficit in Alzheimer’s disease. Ann Neurol 32:371–375. doi:10.1002/ana.410320311
Stern Y, Gurland B, Tatemichi TK, Tang MX, Wilder D, Mayeux R (1994) Influence of education and occupation on the incidence of Alzheimer’s disease. JAMA 271:1004–1010
Stern Y, Albert S, Tang MX, Tsai WY (1999) Rate of memory decline in AD is related to education and occupation: cognitive reserve? Neurology 53:1942–1947
Stern MJ, Fader JJ, Katz MB (2005) Women and the paradox of economic inequality in the twentieth-century. J Soc Hist 39:65–88
Strauss E, Sherman EMS, Spreen O (2006) A Compendium of neuropsychological tests: administration, norms, and commentary. Oxford University Press, New York
Tang X, Oishi K, Faria AV, Hillis AE, Albert MS, Mori S, Miller MI (2013) Bayesian parameter estimation and segmentation in the multi-atlas random orbit model. PLoS One 8:e65591. doi:10.1371/journal.pone.0065591
Tang X, Holland D, Dale AM, Younes L, Miller MI, For the Alzheimer’s Disease Neuroimaging Initiative (2014) Shape abnormalities of subcortical and ventricular structures in mild cognitive impairment and Alzheimer’s disease: detecting, quantifying, and predicting. Hum Brain Mapp 35:3701–3725. doi:10.1002/hbm.22431
Tang X, Crocetti D, Kutten K, Ceritoglu C, Albert MS, Mori S, Mostofsky SH, Miller MI (2015a) Segmentation of brain magnetic resonance images based on multi-atlas likelihood fusion: testing using data with a broad range of anatomical and photometric profiles. Front Neurosci 9:61. doi:10.3389/fnins.2015.00061
Tang X, Holland D, Dale AM, Younes L, Miller MI (2015b) Baseline shape diffeomorphometry patterns of subcortical and ventricular structures in predicting conversion of mild cognitive impairment to Alzheimer’s disease. J Alzheimers Dis 44:599–611. doi:10.3233/JAD-141605
Tang X, Holland D, Dale AM, Younes L, Miller MI, For the Alzheimer’s Disease Neuroimaging Initiative (2015c) The diffeomorphometry of regional shape change rates and its relevance to cognitive deterioration in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp. doi:10.1002/hbm.22758
Thompson PM, Hayashi KM, De Zubicaray GI, Janke AL, Rose SE, Semple J, Hong MS, Herman DH, Gravano D, Doddrell DM et al (2004) Mapping hippocampal and ventricular change in Alzheimer disease. Neuroimage 22:1754–1766. doi:10.1016/j.neuroimage.2004.03.040
Tondelli M, Wilcock GK, Nichelli P, De Jager CA, Jenkinson M, Zamboni G (2012) Structural MRI changes detectable up to ten years before clinical Alzheimer’s disease. Neurobiol Aging 33:825.e25–825.e36. doi:10.1016/j.neurobiolaging.2011.05.018
Tucker AM, Stern Y (2011) Cognitive reserve in aging. Curr Alzheimer Res 8:354–360 (pii BSP/CAR/0126)
Vaillant M, Glaunès J (2005) Surface matching via currents. Inf Process Med Imaging: 381–392
Wang L, Miller JP, Gado MH, McKeel DW, Rothermich M, Miller MI, Morris JC, Csernansky JG (2006) Abnormalities of hippocampal surface structure in very mild dementia of the Alzheimer type. Neuroimage 30:52–60 (pii S1053-8119(05)00716-0)
Wilkinson GS (1993) Wide range achievement test: WRAT3. Wide Range
Wolf H, Kruggel F, Hensel A, Wahlund L, Arendt T, Gertz H (2003) The relationship between head size and intracranial volume in elderly subjects. Brain Res 973:74–80. doi:10.1016/S0006-8993(03)02552-6
Yesavage JA, Brink T, Rose TL, Lum O, Huang V, Adey M, Leirer VO (1983) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17:37–49
Yesavage J, Brink T, Rose T (2000) Geriatric depression scale (GDS) Handbook of psychiatric measures. American Psychiatric Association, Washington DC, pp 544–546
Zahodne LB, Stern Y, Manly JJ (2014) Differing effects of education on cognitive decline in diverse elders with low versus high educational attainment
Acknowledgments
The authors acknowledge the contribution of all participants who gave their time to be involved in this study. Without their service and contributions, this research would not be possible. We would also like to acknowledge Timothy Brown for manually creating the hippocampus and the amygdala segmentations of the 16 atlases used in automatically segmenting the 110 MRI scans of this study. This study was supported by the Johns Hopkins Neurobehavioral Research Unit and a supplement from the National Institute on Aging (BSR Grant P01 AG027735-03). This study was also partially supported by the National Institute of Health/National Institute of Biomedical Imaging and Bioengineering P41 EB015909. Xiaoying Tang is supported by the National Natural Science Foundation of China (81501546) and the SYSU-CMU Shunde International Joint Research Institute Start-up Grant (20150306). Vijay R. Varma was supported by a fellowship from the Epidemiology and Biostatistics of Aging Training Grant (5T32AG000247). Michael I. Miller owns an equal share in Anatomyworks LLC. The terms of this arrangement have been reviewed and approved by the Johns Hopkins University, in accordance with it conflict of interest policy.
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Tang, X., Varma, V.R., Miller, M.I. et al. Education is associated with sub-regions of the hippocampus and the amygdala vulnerable to neuropathologies of Alzheimer’s disease. Brain Struct Funct 222, 1469–1479 (2017). https://doi.org/10.1007/s00429-016-1287-9
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DOI: https://doi.org/10.1007/s00429-016-1287-9