Login Register Cart 0
Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Research Article

Volumetric MRI Demonstrates Atrophy of the Olfactory Cortex in AD

Author(s): Majed Al-Otaibi, Melissa Lessard-Beaudoin, Christian-Alexandre Castellano, Denis Gris, Stephen C. Cunnane and Rona K. Graham*

Volume 17, Issue 10, 2020

Page: [904 - 915] Pages: 12

DOI: 10.2174/1567205017666201215120909

Price: $65

Abstract

Objective: Alzheimer disease (AD) is a chronic neurodegenerative disorder that affects millions of individuals worldwide. Symptoms include memory dysfunction and deficits in attention, planning, language, and overall cognitive function. Olfactory dysfunction is a common symptom of AD and evidence supports that it is an early marker. Furthermore, olfactory bulb and entorhinal cortex atrophy are well described in AD. However, in AD, no studies have assessed the olfactory cortex as a whole and if sex effects are observed.

Methods: Magnetic Resonance Imaging was used to scan 39 participants with an average age of 72 years and included men and women. AAL Single-Subject Atlas (implemented in PNEURO tool - PMOD 3.8) was used to determine the volume of the olfactory cortex and the hippocampus. Olfactory cortex volume was lower in both men and women AD cases compared with controls. This decrease was more apparent in the left olfactory cortex and was influenced by age. As expected, hippocampal volume was also significantly reduced in AD. However, this was only observed in the male cohort. A significant correlation was observed between levels of education and hippocampal volume in controls that were not detected in the AD participants. Asymmetry was observed in the olfactory cortex volume when comparing left and right volumes in both the control and AD participants, which was not observed in the hippocampus.

Results: These data highlight the importance of the role of olfactory cortical atrophy in the pathogenesis of AD and the interplay between the olfactory deficits and degeneration of olfactory regions in the brain.

Keywords: Alzheimer disease, olfactory cortex, atrophy, brain asymmetry, hippocampus, magnetic resonance imaging.

« Previous Next »
[1]
Cermakova P, Eriksdotter M, Lund LH, Winblad B, Religa P, Religa D. Heart failure and Alzheimer’s disease. J Intern Med 2015; 277(4): 406-25.
[http://dx.doi.org/10.1111/joim.12287 ] [PMID: 25041352]
[2]
Gao HM, Hong JS. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 2008; 29(8): 357-65.
[http://dx.doi.org/10.1016/j.it.2008.05.002 ] [PMID: 18599350]
[3]
de la Monte SM, Wands JR. Alzheimer-associated neuronal thread protein mediated cell death is linked to impaired insulin signaling. J Alzheimers Dis 2004; 6(3): 231-42.
[http://dx.doi.org/10.3233/JAD-2004-6304 ] [PMID: 15201478]
[4]
Niikura T, Tajima H, Kita Y. Neuronal cell death in Alzheimer’s disease and a neuroprotective factor, humanin. Curr Neuropharmacol 2006; 4(2): 139-47.
[http://dx.doi.org/10.2174/157015906776359577 ] [PMID: 18615127]
[5]
Doty RL, Perl DP, Steele JC, et al. Olfactory dysfunction in three neurodegenerative diseases. Geriatrics 1991; 46(1): 47-51.
[PMID: 1894145]
[6]
Ruan Y, Zheng XY, Zhang HL, Zhu W, Zhu J. Olfactory dysfunctions in neurodegenerative disorders. J Neurosci Res 2012; 90(9): 1693-700.
[http://dx.doi.org/10.1002/jnr.23054 ] [PMID: 22674288]
[7]
Djordjevic J, Jones-Gotman M, De Sousa K, Chertkow H. Olfaction in patients with mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 2008; 29(5): 693-706.
[http://dx.doi.org/10.1016/j.neurobiolaging.2006.11.014 ] [PMID: 17207898]
[8]
Godoy MD, Voegels RL, Pinna Fde R, Imamura R, Farfel JM. Olfaction in neurologic and neurodegenerative diseases: a literature review. Int Arch Otorhinolaryngol 2015; 19(2): 176-9.
[PMID: 25992176]
[9]
Morris JC, Storandt M, Miller JP, et al. Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 2001; 58(3): 397-405.
[http://dx.doi.org/10.1001/archneur.58.3.397 ] [PMID: 11255443]
[10]
Zhang C, Wang X. Initiation of the age-related decline of odor identification in humans: a meta-analysis. Ageing Res Rev 2017; 40: 45-50.
[http://dx.doi.org/10.1016/j.arr.2017.08.004 ] [PMID: 28830800]
[11]
Larsson M, Finkel D, Pedersen NL. Odor identification: influences of age, gender, cognition, and personality. J Gerontol B Psychol Sci Soc Sci 2000; 55(5): 304-10.
[http://dx.doi.org/10.1093/geronb/55.5.P304 ] [PMID: 10985295]
[12]
Doty RL. Olfactory dysfunction in neurodegenerative diseases: is there a common pathological substrate? Lancet Neurol 2017; 16(6): 478-88.
[http://dx.doi.org/10.1016/S1474-4422(17)30123-0 ] [PMID: 28504111]
[13]
Pearson RC, Esiri MM, Hiorns RW, Wilcock GK, Powell TP. Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. Proc Natl Acad Sci USA 1985; 82(13): 4531-4.
[http://dx.doi.org/10.1073/pnas.82.13.4531 ] [PMID: 3859874]
[14]
Vasavada MM, Wang J, Eslinger PJ, et al. Olfactory cortex degeneration in Alzheimer’s disease and mild cognitive impairment. J Alzheimers Dis 2015; 45(3): 947-58.
[http://dx.doi.org/10.3233/JAD-141947 ] [PMID: 25633674]
[15]
Thomann PA, Dos Santos V, Seidl U, Toro P, Essig M, Schröder J. MRI-derived atrophy of the olfactory bulb and tract in mild cognitive impairment and Alzheimer’s disease. J Alzheimers Dis 2009; 17(1): 213-21.
[http://dx.doi.org/10.3233/JAD-2009-1036 ] [PMID: 19494444]
[16]
Arnold SE, Lee EB, Moberg PJ, et al. Olfactory epithelium amyloid-beta and paired helical filament-tau pathology in Alzheimer disease. Ann Neurol 2010; 67(4): 462-9.
[http://dx.doi.org/10.1002/ana.21910 ] [PMID: 20437581]
[17]
Pini L, Pievani M, Bocchetta M, et al. Brain atrophy in Alzheimer’s Disease and aging. Ageing Res Rev 2016; 30: 25-48.
[http://dx.doi.org/10.1016/j.arr.2016.01.002 ] [PMID: 26827786]
[18]
Devanand DP, Bansal R, Liu J, Hao X, Pradhaban G, Peterson BS. MRI hippocampal and entorhinal cortex mapping in predicting conversion to Alzheimer’s disease. Neuroimage 2012; 60(3): 1622-9.
[http://dx.doi.org/10.1016/j.neuroimage.2012.01.075 ] [PMID: 22289801]
[19]
Du AT, Schuff N, Kramer JH, et al. Higher atrophy rate of entorhinal cortex than hippocampus in AD. Neurology 2004; 62(3): 422-7.
[http://dx.doi.org/10.1212/01.WNL.0000106462.72282.90 ] [PMID: 14872024]
[20]
Dubois B, Feldman HH, Jacova C, et al. Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 2007; 6(8): 734-46.
[http://dx.doi.org/10.1016/S1474-4422(07)70178-3 ] [PMID: 17616482]
[21]
Johnson KA, Fox NC, Sperling RA, Klunk WE. Brain imaging in Alzheimer disease. Cold Spring Harb Perspect Med 2012; 2(4): a006213.
[http://dx.doi.org/10.1101/cshperspect.a006213 ] [PMID: 22474610]
[22]
Henneman WJ, Sluimer JD, Barnes J, et al. Hippocampal atrophy rates in Alzheimer disease: added value over whole brain volume measures. Neurology 2009; 72(11): 999-1007.
[http://dx.doi.org/10.1212/01.wnl.0000344568.09360.31 ] [PMID: 19289740]
[23]
Christen-Zaech S, Kraftsik R, Pillevuit O, et al. Early olfactory involvement in Alzheimer’s disease. Can J Neurol Sci 2003; 30(1): 20-5.
[http://dx.doi.org/10.1017/S0317167100002389 ] [PMID: 12619779]
[24]
Wilson RS, Schneider JA, Arnold SE, Tang Y, Boyle PA, Bennett DA. Olfactory identification and incidence of mild cognitive impairment in older age. Arch Gen Psychiatry 2007; 64(7): 802-8.
[http://dx.doi.org/10.1001/archpsyc.64.7.802 ] [PMID: 17606814]
[25]
Bahar-Fuchs A, Chételat G, Villemagne VL, et al. Olfactory deficits and amyloid-β burden in Alzheimer’s disease, mild cognitive impairment, and healthy aging: a PiB PET study. J Alzheimers Dis 2010; 22(4): 1081-7.
[http://dx.doi.org/10.3233/JAD-2010-100696 ] [PMID: 20930316]
[26]
Carvalho DZ, St Louis EK, Knopman DS, et al. Association of excessive daytime sleepiness with longitudinal β-amyloid accumulation in elderly persons without dementia. JAMA Neurol 2018; 75(6): 672-80.
[http://dx.doi.org/10.1001/jamaneurol.2018.0049 ] [PMID: 29532057]
[27]
Kovács T, Cairns NJ, Lantos PL. Olfactory centres in Alzheimer’s disease: olfactory bulb is involved in early Braak’s stages. Neuroreport 2001; 12(2): 285-8.
[http://dx.doi.org/10.1097/00001756-200102120-00021 ] [PMID: 11209936]
[28]
Lazarov O, Marr RA. Neurogenesis and Alzheimer’s disease: at the crossroads. Exp Neurol 2010; 223(2): 267-81.
[http://dx.doi.org/10.1016/j.expneurol.2009.08.009 ] [PMID: 19699201]
[29]
Foveau B, Albrecht S, Bennett DA, Correa JA, LeBlanc AC. Increased Caspase-6 activity in the human anterior olfactory nuclei of the olfactory bulb is associated with cognitive impairment. Acta Neuropathol Commun 2016; 4(1): 127.
[http://dx.doi.org/10.1186/s40478-016-0400-x ] [PMID: 27931265]
[30]
LeBlanc AC. Caspase-6 as a novel early target in the treatment of Alzheimer’s disease. Eur J Neurosci 2013; 37(12): 2005-18.
[http://dx.doi.org/10.1111/ejn.12250 ] [PMID: 23773070]
[31]
Albrecht S, Bourdeau M, Bennett D, Mufson EJ, Bhattacharjee M, LeBlanc AC. Activation of caspase-6 in aging and mild cognitive impairment. Am J Pathol 2007; 170(4): 1200-9.
[http://dx.doi.org/10.2353/ajpath.2007.060974 ] [PMID: 17392160]
[32]
Derflinger S, Sorg C, Gaser C, et al. Grey-matter atrophy in Alzheimer’s disease is asymmetric but not lateralized. J Alzheimers Dis 2011; 25(2): 347-57.
[http://dx.doi.org/10.3233/JAD-2011-110041 ] [PMID: 21422522]
[33]
Toga AW, Thompson PM. Mapping brain asymmetry. Nat Rev Neurosci 2003; 4(1): 37-48.
[http://dx.doi.org/10.1038/nrn1009 ] [PMID: 12511860]
[34]
Donix M, Burggren AC, Scharf M, et al. APOE associated hemispheric asymmetry of entorhinal cortical thickness in aging and Alzheimer’s disease. Psychiatry Res 2013; 214(3): 212-20.
[http://dx.doi.org/10.1016/j.pscychresns.2013.09.006 ] [PMID: 24080518]
[35]
Thompson PM, Hayashi KM, Dutton RA, et al. Tracking Alzheimer’s disease. Ann N Y Acad Sci 2007; 1097: 183-214.
[http://dx.doi.org/10.1196/annals.1379.017 ] [PMID: 17413023]
[36]
Garcia-Falgueras A, Junque C, Giménez M, Caldú X, Segovia S, Guillamon A. Sex differences in the human olfactory system. Brain Res 2006; 1116(1): 103-11.
[http://dx.doi.org/10.1016/j.brainres.2006.07.115 ] [PMID: 16942757]
[37]
Croteau E, Castellano CA, Fortier M, et al. A cross-sectional comparison of brain glucose and ketone metabolism in cognitively healthy older adults, mild cognitive impairment and early Alzheimer’s disease. Exp Gerontol 2018; 107: 18-26.
[http://dx.doi.org/10.1016/j.exger.2017.07.004 ] [PMID: 28709938]
[38]
McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 2011; 7(3): 263-9.
[http://dx.doi.org/10.1016/j.jalz.2011.03.005 ] [PMID: 21514250]
[39]
Castellano CA, Paquet N, Dionne IJ, et al. A 3-month aerobic training program improves brain energy metabolism in mild alzheimer’s disease: preliminary results from a neuroimaging study. J Alzheimers Dis 2017; 56(4): 1459-68.
[http://dx.doi.org/10.3233/JAD-161163 ] [PMID: 28157102]
[40]
Rolls ET, Joliot M, Tzourio-Mazoyer N. Implementation of a new parcellation of the orbitofrontal cortex in the automated anatomical labeling atlas. Neuroimage 2015; 122: 1-5.
[http://dx.doi.org/10.1016/j.neuroimage.2015.07.075 ] [PMID: 26241684]
[41]
Anatomie des Centres Nerveux. Am J Psychiatry 1895; 51(3): 402-3.
[http://dx.doi.org/10.1176/ajp.51.3.402]
[42]
Fjaeldstad A, Fernandes HM, Van Hartevelt TJ, et al. Brain fingerprints of olfaction: a novel structural method for assessing olfactory cortical networks in health and disease. Sci Rep 2017; 7: 42534.
[http://dx.doi.org/10.1038/srep42534 ] [PMID: 28195241]
[43]
Hyatt CS, Owens MM, Crowe ML, Carter NT, Lynam DR, Miller JD. The quandary of covarying: a brief review and empirical examination of covariate use in structural neuroimaging studies on psychological variables. Neuroimage 2020; 205: 116225.
[http://dx.doi.org/10.1016/j.neuroimage.2019.116225 ] [PMID: 31568872]
[44]
Conti MZ, Vicini-Chilovi B, Riva M, et al. Odor identification deficit predicts clinical conversion from mild cognitive impairment to dementia due to Alzheimer’s disease. Arch Clin Neuropsychol 2013; 28(5): 391-9.
[http://dx.doi.org/10.1093/arclin/act032]
[45]
Buschhüter D, Smitka M, Puschmann S, et al. Correlation between olfactory bulb volume and olfactory function. Neuroimage 2008; 42(2): 498-502.
[http://dx.doi.org/10.1016/j.neuroimage.2008.05.004 ] [PMID: 18555701]
[46]
Li W, Howard JD, Gottfried JA. Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer’s disease. Brain 2010; 133(9): 2714-26.
[http://dx.doi.org/10.1093/brain/awq209 ] [PMID: 20724290]
[47]
Harper L, Bouwman F, Burton EJ, et al. Patterns of atrophy in pathologically confirmed dementias: a voxelwise analysis. J Neurol Neurosurg Psychiatry 2017; 88(11): 908-16.
[http://dx.doi.org/10.1136/jnnp-2016-314978 ] [PMID: 28473626]
[48]
Juottonen K, Laakso MP, Insausti R, et al. Volumes of the entorhinal and perirhinal cortices in Alzheimer’s disease. Neurobiol Aging 1998; 19(1): 15-22.
[http://dx.doi.org/10.1016/S0197-4580(98)00007-4 ] [PMID: 9562498]
[49]
Du AT, Schuff N, Amend D, et al. Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer’s disease. J Neurol Neurosurg Psychiatry 2001; 71(4): 441-7.
[http://dx.doi.org/10.1136/jnnp.71.4.441 ] [PMID: 11561025]
[50]
Westervelt HJ, Bruce JM, Coon WG, Tremont G. Odor identification in mild cognitive impairment subtypes. J Clin Exp Neuropsychol 2008; 30(2): 151-6.
[http://dx.doi.org/10.1080/13803390701287408 ] [PMID: 18938667]
[51]
Loewenstein DA, Barker WW, Chang JY, et al. Predominant left hemisphere metabolic dysfunction in dementia. Arch Neurol 1989; 46(2): 146-52.
[http://dx.doi.org/10.1001/archneur.1989.00520380046012 ] [PMID: 2783845]
[52]
Barnes J, Scahill RI, Schott JM, Frost C, Rossor MN, Fox NC. Does Alzheimer’s disease affect hippocampal asymmetry? Evidence from a cross-sectional and longitudinal volumetric MRI study. Dement Geriatr Cogn Disord 2005; 19(5-6): 338-44.
[http://dx.doi.org/10.1159/000084560 ] [PMID: 15785035]
[53]
Zhao W, Wang X, Yin C, He M, Li S, Han Y. Trajectories of the hippocampal subfields atrophy in the Alzheimer’s disease: a structural imaging study. Front Neuroinform 2019; 13: 13.
[http://dx.doi.org/10.3389/fninf.2019.00013 ] [PMID: 30983985]
[54]
Mueller SG, Schuff N, Yaffe K, Madison C, Miller B, Weiner MW. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp 2010; 31(9): 1339-47.
[http://dx.doi.org/10.1002/hbm.20934 ] [PMID: 20839293]
[55]
Apostolova LG, Dinov ID, Dutton RA, et al. 3D comparison of hippocampal atrophy in amnestic mild cognitive impairment and Alzheimer’s disease. Brain 2006; 129(Pt 11): 2867-73.
[http://dx.doi.org/10.1093/brain/awl274 ] [PMID: 17018552]
[56]
Laakso MP, Lehtovirta M, Partanen K, Riekkinen PJ, Soininen H. Hippocampus in Alzheimer’s disease: a 3-year follow-up MRI study. Biol Psychiatry 2000; 47(6): 557-61.
[http://dx.doi.org/10.1016/S0006-3223(99)00167-5 ] [PMID: 10715362]
[57]
Murphy C, Jernigan TL, Fennema-Notestine C. Left hippocampal volume loss in Alzheimer’s disease is reflected in performance on odor identification: a structural MRI study. J Int Neuropsychol Soc 2003; 9(3): 459-71.
[http://dx.doi.org/10.1017/S1355617703930116 ] [PMID: 12666770]
[58]
Pievani M, Galluzzi S, Thompson PM, Rasser PE, Bonetti M, Frisoni GB. APOE4 is associated with greater atrophy of the hippocampal formation in Alzheimer’s disease. Neuroimage 2011; 55(3): 909-19.
[http://dx.doi.org/10.1016/j.neuroimage.2010.12.081 ] [PMID: 21224004]
[59]
Lindgren L, Bergdahl J, Nyberg L. Longitudinal evidence for smaller hippocampus volume as a vulnerability factor for perceived stress. Cereb Cortex 2016; 26(8): 3527-33.
[http://dx.doi.org/10.1093/cercor/bhw154 ] [PMID: 27230217]
[60]
Mathias SR, Knowles EE, Kent JW Jr, et al. Recurrent major depression and right hippocampal volume: a bivariate linkage and association study. Hum Brain Mapp 2016; 37(1): 191-202.
[http://dx.doi.org/10.1002/hbm.23025 ] [PMID: 26485182]
[61]
Fisher DW, Bennett DA, Dong H. Sexual dimorphism in predisposition to Alzheimer’s disease. Neurobiol Aging 2018; 70: 308-24.
[http://dx.doi.org/10.1016/j.neurobiolaging.2018.04.004 ] [PMID: 29754747]
[62]
Ferreira D, Verhagen C, Hernández-Cabrera JA, et al. Distinct subtypes of Alzheimer’s disease based on patterns of brain atrophy: longitudinal trajectories and clinical applications. Sci Rep 2017; 7: 46263.
[http://dx.doi.org/10.1038/srep46263 ] [PMID: 28417965]
[63]
Hanna Al-Shaikh FS, Duara R, Crook JE, et al. Selective vulnerability of the nucleus basalis of meynert among neuropathologic subtypes of Alzheimer disease. JAMA Neurol 2020; 77(2): 225-33.
[PMID: 31657834]
[64]
Murray ME, Graff-Radford NR, Ross OA, Petersen RC, Duara R, Dickson DW. Neuropathologically defined subtypes of Alzheimer’s disease with distinct clinical characteristics: a retrospective study. Lancet Neurol 2011; 10(9): 785-96.
[http://dx.doi.org/10.1016/S1474-4422(11)70156-9 ] [PMID: 21802369]
[65]
Kong V, Devenyi GA, Gallino D, et al. Early-in-life neuroanatomical and behavioural trajectories in a triple transgenic model of Alzheimer’s disease. Brain Struct Funct 2018; 223(7): 3365-82.
[http://dx.doi.org/10.1007/s00429-018-1691-4 ] [PMID: 29948190]
[66]
Yu HL, Chen ZJ, Zhao JW, Duan SR, Zhao JK. Olfactory impairment and hippocampal volume in a Chinese MCI clinical sample. Alzheimer Dis Assoc Disord 2019; 33(2): 124-8.
[http://dx.doi.org/10.1097/WAD.0000000000000305 ] [PMID: 31094709]
[67]
Liang X, Yin Z, Liu R, et al. The role of MRI biomarkers and their interactions with cognitive status and APOE ε4 in nondemented elderly subjects. Neurodegener Dis 2018; 18(5-6): 270-80.
[http://dx.doi.org/10.1159/000495754 ] [PMID: 30673663]
[68]
Kelly DA, Seidenberg M, Reiter K, et al. Differential 5-year brain atrophy rates in cognitively declining and stable APOE-ε4 elders. Neuropsychology 2018; 32(6): 647-53.
[http://dx.doi.org/10.1037/neu0000444 ] [PMID: 29911873]
[69]
Low A, Ng KP, Chander RJ, Wong B, Kandiah N. Association of asymmetrical white matter hyperintensities and apolipoprotein E4 on cognitive impairment. J Alzheimers Dis 2019; 70(3): 953-64.
[http://dx.doi.org/10.3233/JAD-190159 ] [PMID: 31306121]
[70]
Abraham M, Seidenberg M, Kelly DA, et al. Episodic memory and hippocampal volume predict 5-year mild cognitive impairment conversion in healthy apolipoprotein ε4 carriers. J Int Neuropsychol Soc 2020; 26(7): 733-8.
[http://dx.doi.org/10.1017/S1355617720000181 ] [PMID: 32131913]
[71]
Stamps JJ, Bartoshuk LM, Heilman KM. A brief olfactory test for Alzheimer’s disease. J Neurol Sci 2013; 333(1-2): 19-24.
[http://dx.doi.org/10.1016/j.jns.2013.06.033 ] [PMID: 23927938]
[72]
Nobis L, Manohar SG, Smith SM, et al. Hippocampal volume across age: Nomograms derived from over 19,700 people in UK Biobank. Neuroimage Clin 2019; 23: 101904.
[http://dx.doi.org/10.1016/j.nicl.2019.101904 ] [PMID: 31254939]
[73]
Pedraza O, Bowers D, Gilmore R. Asymmetry of the hippocampus and amygdala in MRI volumetric measurements of normal adults. J Int Neuropsychol Soc 2004; 10(5): 664-78.
[http://dx.doi.org/10.1017/S1355617704105080 ] [PMID: 15327714]
[74]
Geroldi C, Laakso MP, DeCarli C, et al. Apolipoprotein E genotype and hippocampal asymmetry in Alzheimer’s disease: a volumetric MRI study. J Neurol Neurosurg Psychiatry 2000; 68(1): 93-6.
[http://dx.doi.org/10.1136/jnnp.68.1.93 ] [PMID: 10601411]
[75]
Peters R. Ageing and the brain. Postgrad Med J 2006; 82(964): 84-8.
[http://dx.doi.org/10.1136/pgmj.2005.036665 ] [PMID: 16461469]
[76]
Noble KG, Grieve SM, Korgaonkar MS, et al. Hippocampal volume varies with educational attainment across the life-span. Front Hum Neurosci 2012; 6: 307.
[http://dx.doi.org/10.3389/fnhum.2012.00307 ] [PMID: 23162453]
[77]
Evans GW. The environment of childhood poverty. Am Psychol 2004; 59(2): 77-92.
[http://dx.doi.org/10.1037/0003-066X.59.2.77 ] [PMID: 14992634]
[78]
Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002; 8(3): 448-60.
[http://dx.doi.org/10.1017/S1355617702813248 ] [PMID: 11939702]
[79]
Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord 2006; 20(3)(Suppl. 2): S69-74.
[http://dx.doi.org/10.1097/00002093-200607001-00010 ] [PMID: 16917199]
[80]
Wilson DA, Kadohisa M, Fletcher ML. Cortical contributions to olfaction: plasticity and perception. Semin Cell Dev Biol 2006; 17(4): 462-70.
[http://dx.doi.org/10.1016/j.semcdb.2006.04.008 ] [PMID: 16750923]
[81]
Wilson DA, Stevenson RJ. The fundamental role of memory in olfactory perception. Trends Neurosci 2003; 26(5): 243-7.
[http://dx.doi.org/10.1016/S0166-2236(03)00076-6 ] [PMID: 12744840]

Rights & Permissions Print Cite
Article Metrics
31
© 2024 Bentham Science Publishers | Privacy Policy