Brain Topography

, Volume 25, Issue 4, pp 431–442

The Influence of Apolipoprotein E Epsilon4 Polymorphism on qEEG Profiles in Healthy Young Females: A Resting EEG Study

  • Tien-Wen Lee
  • Younger W.-Y. Yu
  • Chen-Jee Hong
  • Shih-Jen Tsai
  • Hung-Chi Wu
  • Tai-Jui Chen
Original Paper

Abstract

The epsilon4 allele of the Apolipoprotein E (ApoE) gene has been linked to various neurological conditions and the aging process in the elderly. However, evidence has suggested that the influence of ApoE epsilon4 may commence in early life. This study examined the modulatory effects of ApoE epsilon4 on regional neural activity as well as inter-regional neural interactions in a young population aged 19–21. Blood samples and resting state eyes-closed EEG signals were collected from 265 healthy females, and stratified into two groups: epsilon4 carriers and non-carriers. The values of the log-transformed mean power of 18 electrodes and the mutual information of 20 channel pairs across delta, theta, alpha and beta frequencies were analyzed. Our connectivity analysis was based on information theory, which combined Morlet wavelet transform and mutual information calculation. Between-group statistics were performed by independent t-test. We notice a consistent trend across the brain, in which ApoE epsilon4 carriers possess lower regional power at the alpha band. The epsilon4 allele is also associated with lower regional power at the theta frequency in the left frontal and posterior brain regions. Functional connectivity analyses reveal a right-lateralized network that differentiates epsilon4 carriers and non-carriers, with lower connectivity strengths for the former. Our tonic EEG analyses complement those of previous reports in that the ApoE epsilon4 allele has a negative impact on regional neural synchronization and inter-regional neural interaction.

Keywords

Electroencephalography (EEG) Power spectrum Mutual information Apolipoprotein E (ApoE) Genetic polymorphism 

References

  1. Alexander DM, Williams LM, Gatt JM, Dobson-Stone C, Kuan SA, Todd EG, Schofield PR, Cooper NJ, Gordon E (2007) The contribution of apolipoprotein E alleles on cognitive performance and dynamic neural activity over six decades. Biol Psychol 75(3):229–238PubMedCrossRefGoogle Scholar
  2. Anderson GD, Temkin NR, Dikmen SS, Diaz-Arrastia R, Machamer JE, Farhrenbruch C, Miller JW, Sadrzadeh SM (2009) Haptoglobin phenotype and apolipoprotein E polymorphism: relationship to posttraumatic seizures and neuropsychological functioning after traumatic brain injury. Epilepsy Behav 16(3):501–506PubMedCrossRefGoogle Scholar
  3. Ariza M, Pueyo R, Matarin MM, Junque C, Mataro M, Clemente I, Moral P, Poca MA, Garnacho A, Sahuquillo J (2006) Influence of APOE polymorphism on cognitive and behavioural outcome in moderate and severe traumatic brain injury. J Neurol Neurosurg Psychiatry 77(10):1191–1193PubMedCrossRefGoogle Scholar
  4. Babiloni C, Benussi L, Binetti G, Cassetta E, Dal GF, Del Percio C, Ferreri F, Ferri R, Frisoni G, Ghidoni R, Miniussi C, Rodriguez G, Romani GL, Squitti R, Ventriglia MC, Rossini PM (2006) Apolipoprotein E and alpha brain rhythms in mild cognitive impairment: a multicentric electroencephalogram study. Ann Neurol 59(2):323–334PubMedCrossRefGoogle Scholar
  5. Bartres-Faz D, Junque C, Lopez-Alomar A, Valveny N, Moral P, Casamayor R, Salido A, Bel C, Clemente IC (2001) Neuropsychological and genetic differences between age-associated memory impairment and mild cognitive impairment entities. J Am Geriatr Soc 49(7):985–990PubMedCrossRefGoogle Scholar
  6. Bennett DA, De Jager PL, Leurgans SE, Schneider JA (2009) Neuropathologic intermediate phenotypes enhance association to Alzheimer susceptibility alleles. Neurology 72(17):1495–1503PubMedCrossRefGoogle Scholar
  7. Biffi A, Anderson CD, Desikan RS, Sabuncu M, Cortellini L, Schmansky N, Salat D, Rosand J (2010) Genetic variation and neuroimaging measures in Alzheimer disease. Arch Neurol 67(6):677–685PubMedCrossRefGoogle Scholar
  8. Bondi MW, Salmon DP, Monsch AU, Galasko D, Butters N, Klauber MR, Thal LJ, Saitoh T (1995) Episodic memory changes are associated with the APOE-epsilon 4 allele in nondemented older adults. Neurology 45(12):2203–2206PubMedCrossRefGoogle Scholar
  9. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW (2000) Patterns of brain activation in people at risk for Alzheimer’s disease. N Engl J Med 343(7):450–456PubMedCrossRefGoogle Scholar
  10. Brignani D, Maioli C, Maria PR, Miniussi C (2007) Event-related power modulations of brain activity preceding visually guided saccades. Brain Res 1136(1):122–131PubMedCrossRefGoogle Scholar
  11. Buckholtz JW, Sust S, Tan HY, Mattay VS, Straub RE, Meyer-Lindenberg A, Weinberger DR, Callicott JH (2007) fMRI evidence for functional epistasis between COMT and RGS4. Mol Psychiatry 12(10):885, 893–895Google Scholar
  12. Cacabelos R (2008) Pharmacogenomics in Alzheimer’s disease. Methods Mol Biol 448:213–357PubMedCrossRefGoogle Scholar
  13. Caccamo A, Fisher A, LaFerla FM (2009) M1 agonists as a potential disease-modifying therapy for Alzheimer’s disease. Curr Alzheimer Res 6(2):112–117PubMedCrossRefGoogle Scholar
  14. Caldu X, Vendrell P, Bartres-Faz D, Clemente I, Bargallo N, Jurado MA, Serra-Grabulosa JM, Junque C (2007) Impact of the COMT Val108/158 Met and DAT genotypes on prefrontal function in healthy subjects. Neuroimage 37(4):1437–1444PubMedCrossRefGoogle Scholar
  15. Chen CC, Hsieh JC, Wu YZ, Lee PL, Chen SS, Niddam DM, Yeh TC, Wu YT (2008) Mutual-information-based approach for neural connectivity during self-paced finger lifting task. Hum Brain Mapp 29(3):265–280PubMedCrossRefGoogle Scholar
  16. Coben LA, Chi D, Snyder AZ, Storandt M (1990) Replication of a study of frequency analysis of the resting awake EEG in mild probable Alzheimer’s disease. Electroencephalogr Clin Neurophysiol 75(3):148–154PubMedCrossRefGoogle Scholar
  17. da Silva FHL, Pijn JP, Velis D, Nijssen PC (1997) Alpha rhythms: noise, dynamics and models. Int J Psychophysiol 26(1–3):237–249CrossRefGoogle Scholar
  18. Danos P, Guich S, Abel L, Buchsbaum MS (2001) Eeg alpha rhythm and glucose metabolic rate in the thalamus in schizophrenia. Neuropsychobiology 43(4):265–272PubMedCrossRefGoogle Scholar
  19. Del Bo R, Comi GP, Giorda R, Crimi M, Locatelli F, Martinelli-Boneschi F, Pozzoli U, Castelli E, Bresolin N, Scarlato G (2003) The 129 codon polymorphism of the prion protein gene influences earlier cognitive performance in Down syndrome subjects. J Neurol 250(6):688–692PubMedCrossRefGoogle Scholar
  20. Donix M, Burggren AC, Suthana NA, Siddarth P, Ekstrom AD, Krupa AK, Jones M, Rao A, Martin-Harris L, Ercoli LM, Miller KJ, Small GW, Bookheimer SY (2010) Longitudinal changes in medial temporal cortical thickness in normal subjects with the APOE-4 polymorphism. Neuroimage 53(1):37–43PubMedCrossRefGoogle Scholar
  21. Draca S (2010) Gender-specific functional cerebral asymmetries and unilateral cerebral lesion sequelae. Rev Neurosci 21(6):421–425PubMedCrossRefGoogle Scholar
  22. Duffy FH, Lyer G, Surwillo WW (1989) Clinical electroencephalography and topographical brain mapping. Springer-Verlag, New YorkCrossRefGoogle Scholar
  23. Espeseth T, Greenwood PM, Reinvang I, Fjell AM, Walhovd KB, Westlye LT, Wehling E, Lundervold A, Rootwelt H, Parasuraman R (2006) Interactive effects of APOE and CHRNA4 on attention and white matter volume in healthy middle-aged and older adults. Cogn Affect Behav Neurosci 6(1):31–43PubMedCrossRefGoogle Scholar
  24. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009a) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci USA 106(17):7209–7214PubMedCrossRefGoogle Scholar
  25. Filippini N, Zarei M, Beckmann CF, Galluzzi S, Borsci G, Testa C, Bonetti M, Beltramello A, Ghidoni R, Benussi L, Binetti G, Frisoni GB (2009b) Regional atrophy of transcallosal prefrontal connections in cognitively normal APOE epsilon4 carriers. J Magn Reson Imaging 29(5):1021–1026PubMedCrossRefGoogle Scholar
  26. Fisher A, Brandeis R, Chapman S, Pittel Z, Michaelson DM (1998) M1 muscarinic agonist treatment reverses cognitive and cholinergic impairments of apolipoprotein E-deficient mice. J Neurochem 70(5):1991–1997PubMedCrossRefGoogle Scholar
  27. Forstl H, Sattel H, Sarochan M, Besthom C, Czech C, Daniel S, Geiger-Kabisch C, Hentschel F, Zerfass R, Beyreuther K (1996) Alzheimer dementia and normal aging. Clinical, neuroradiologic, neurophysiologic and molecular biology follow-up data. Nervenarzt 67(9):730–738PubMedCrossRefGoogle Scholar
  28. Forstl H, Bickel H, Frolich L, Gertz HJ, Kurz A, Marksteiner J, Monsch AU, Pantel J, Schmidt R, Schonknecht P (2008) Mild cognitive impairment with predictors of rapid decline. Dtsch Med Wochenschr 133(9):431–436PubMedCrossRefGoogle Scholar
  29. Godin O, Tzourio C, Maillard P, Alperovitch A, Mazoyer B, Dufouil C (2009) Apolipoprotein E genotype is related to progression of white matter lesion load. Stroke 40(10):3186–3190PubMedCrossRefGoogle Scholar
  30. Greenwood PM, Sunderland T, Friz JL, Parasuraman R (2000) Genetics and visual attention: selective deficits in healthy adult carriers of the epsilon 4 allele of the apolipoprotein E gene. Proc Natl Acad Sci USA 97(21):11661–11666PubMedCrossRefGoogle Scholar
  31. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19(1):72–78PubMedCrossRefGoogle Scholar
  32. Henderson AS, Easteal S, Jorm AF, Mackinnon AJ, Korten AE, Christensen H, Croft L, Jacomb PA (1995) Apolipoprotein E allele epsilon 4, dementia, and cognitive decline in a population sample. Lancet 346(8987):1387–1390PubMedCrossRefGoogle Scholar
  33. Hermens DF, Soei EX, Clarke SD, Kohn MR, Gordon E, Williams LM (2005) Resting EEG theta activity predicts cognitive performance in attention-deficit hyperactivity disorder. Pediatr Neurol 32(4):248–256PubMedCrossRefGoogle Scholar
  34. Hoptman MJ, Davidson RJ (1998) Baseline EEG asymmetries and performance on neuropsychological tasks. Neuropsychologia 36(12):1343–1353PubMedCrossRefGoogle Scholar
  35. Hyman BT, Gomez-Isla T, Briggs M, Chung H, Nichols S, Kohout F, Wallace R (1996) Apolipoprotein E and cognitive change in an elderly population. Ann Neurol 40(1):55–66PubMedCrossRefGoogle Scholar
  36. Jelic V, Kowalski J (2009) Evidence-based evaluation of diagnostic accuracy of resting EEG in dementia and mild cognitive impairment. Clin EEG Neurosci 40(2):129–142PubMedCrossRefGoogle Scholar
  37. Jelic V, Julin P, Shigeta M, Nordberg A, Lannfelt L, Winblad B, Wahlund LO (1997) Apolipoprotein E epsilon4 allele decreases functional connectivity in Alzheimer’s disease as measured by EEG coherence. J Neurol Neurosurg Psychiatry 63(1):59–65PubMedCrossRefGoogle Scholar
  38. Jeong J, Gore JC, Peterson BS (2001) Mutual information analysis of the EEG in patients with Alzheimer’s disease. Clin Neurophysiol 112(5):827–835PubMedCrossRefGoogle Scholar
  39. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29(2–3):169–195PubMedCrossRefGoogle Scholar
  40. Klimesch W, Schimke H, Doppelmayr M, Ripper B, Schwaiger J, Pfurtscheller G (1996) Event-related desynchronization (ERD) and the Dm effect: does alpha desynchronization during encoding predict later recall performance? Int J Psychophysiol 24(1–2):47–60PubMedCrossRefGoogle Scholar
  41. Kokubo Y, Chowdhury AH, Date C, Yokoyama T, Sobue H, Tanaka H (2000) Age-dependent association of apolipoprotein E genotypes with stroke subtypes in a Japanese rural population. Stroke 31(6):1299–1306PubMedCrossRefGoogle Scholar
  42. Laufs H, Kleinschmidt A, Beyerle A, Eger E, Salek-Haddadi A, Preibisch C, Krakow K (2003) EEG-correlated fMRI of human alpha activity. Neuroimage 19(4):1463–1476PubMedCrossRefGoogle Scholar
  43. Lehtovirta M, Soininen H, Laakso MP, Partanen K, Helisalmi S, Mannermaa A, Ryynanen M, Kuikka J, Hartikainen P, Riekkinen PJ Sr (1996) SPECT and MRI analysis in Alzheimer’s disease: relation to apolipoprotein E epsilon 4 allele. J Neurol Neurosurg Psychiatry 60(6):644–649PubMedCrossRefGoogle Scholar
  44. Lehtovirta M, Partanen J, Kononen M, Hiltunen J, Helisalmi S, Hartikainen P, Riekkinen P Sr, Soininen H (2000) A longitudinal quantitative EEG study of Alzheimer’s disease: relation to apolipoprotein E polymorphism. Dement Geriatr Cogn Disord 11(1):29–35PubMedCrossRefGoogle Scholar
  45. Li J, Kuang WH, Li J, Wang X, Huang MS, Wu DP (2005) Study of relationship between ApoE epsilon4 allele and hippocampal atrophy in Alzheimer disease. Sichuan Da Xue Xue Bao Yi Xue Ban 36(1):50–52PubMedGoogle Scholar
  46. Liu Y, Laakso MP, Karonen JO, Vanninen RL, Nuutinen J, Soimakallio S, Aronen HJ (2002) Apolipoprotein E polymorphism and acute ischemic stroke: a diffusion- and perfusion-weighted magnetic resonance imaging study. J Cereb Blood Flow Metab 22(11):1336–1342PubMedCrossRefGoogle Scholar
  47. McIntosh AM, Baig BJ, Hall J, Job D, Whalley HC, Lymer GK, Moorhead TW, Owens DG, Miller P, Porteous D, Lawrie SM, Johnstone EC (2007) Relationship of catechol-O-methyltransferase variants to brain structure and function in a population at high risk of psychosis. Biol Psychiatry 61(10):1127–1134PubMedCrossRefGoogle Scholar
  48. Meyer MR, Tschanz JT, Norton MC, Welsh-Bohmer KA, Steffens DC, Wyse BW, Breitner JC (1998) APOE genotype predicts when–not whether–one is predisposed to develop Alzheimer disease. Nat Genet 19(4):321–322PubMedCrossRefGoogle Scholar
  49. Mulert C, Juckel G, Brunnmeier M, Karch S, Leicht G, Mergl R, Moller HJ, Hegerl U, Pogarell O (2007) Prediction of treatment response in major depression: integration of concepts. J Affect Disord 98(3):215–225PubMedCrossRefGoogle Scholar
  50. Neuper C, Grabner RH, Fink A, Neubauer AC (2005) Long-term stability and consistency of EEG event-related (de-)synchronization across different cognitive tasks. Clin Neurophysiol 116(7):1681–1694PubMedCrossRefGoogle Scholar
  51. Niedermeyer E (1990) Alpha-like rhythmical activity of the temporal lobe. Clin Electroencephalogr 21(4):210–224PubMedGoogle Scholar
  52. Niedermeyer E (1997) Alpha rhythms as physiological and abnormal phenomena. Int J Psychophysiol 26(1–3):31–49PubMedCrossRefGoogle Scholar
  53. Nunez PL, Wingeier BM, Silberstein RB (2001) Spatial-temporal structures of human alpha rhythms: theory, microcurrent sources, multiscale measurements, and global binding of local networks. Hum Brain Mapp 13(3):125–164PubMedCrossRefGoogle Scholar
  54. Parasuraman R, Greenwood PM, Sunderland T (2002) The apolipoprotein E gene, attention, and brain function. Neuropsychology 16(2):254–274PubMedCrossRefGoogle Scholar
  55. Pennanen C, Testa C, Boccardi M, Laakso MP, Hallikainen M, Helkala EL, Hanninen T, Kivipelto M, Kononen M, Nissinen A, Tervo S, Vanhanen M, Vanninen R, Frisoni GB, Soininen H (2006) The effect of apolipoprotein polymorphism on brain in mild cognitive impairment: a voxel-based morphometric study. Dement Geriatr Cogn Disord 22(1):60–66PubMedCrossRefGoogle Scholar
  56. Pfurtscheller G, Andrew C (1999) Event-related changes of band power and coherence: methodology and interpretation. J Clin Neurophysiol 16(6):512–519PubMedCrossRefGoogle Scholar
  57. Plassman BL, Welsh-Bohmer KA, Bigler ED, Johnson SC, Anderson CV, Helms MJ, Saunders AM, Breitner JC (1997) Apolipoprotein E epsilon 4 allele and hippocampal volume in twins with normal cognition. Neurology 48(4):985–989PubMedCrossRefGoogle Scholar
  58. Poirier J, Delisle MC, Quirion R, Aubert I, Farlow M, Lahiri D, Hui S, Bertrand P, Nalbantoglu J, Gilfix BM, Gauthier S (1995) Apolipoprotein E4 allele as a predictor of cholinergic deficits and treatment outcome in Alzheimer disease. Proc Natl Acad Sci USA 92(26):12260–12264PubMedCrossRefGoogle Scholar
  59. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, Mahley RW, Mucke L (1998) Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci USA 95(18):10914–10919PubMedCrossRefGoogle Scholar
  60. Raber J, Wong D, Yu GQ, Buttini M, Mahley RW, Pitas RE, Mucke L (2000) Apolipoprotein E and cognitive performance. Nature 404(6776):352–354PubMedCrossRefGoogle Scholar
  61. Raz N, Rodrigue KM, Kennedy KM, Land S (2009) Genetic and vascular modifiers of age-sensitive cognitive skills: effects of COMT, BDNF, ApoE, and hypertension. Neuropsychology 23(1):105–116PubMedCrossRefGoogle Scholar
  62. Reed T, Carmelli D, Swan GE, Breitner JC, Welsh KA, Jarvik GP, Deeb S, Auwerx J (1994) Lower cognitive performance in normal older adult male twins carrying the apolipoprotein E epsilon 4 allele. Arch Neurol 51(12):1189–1192PubMedCrossRefGoogle Scholar
  63. Reiman EM, Caselli RJ, Yun LS, Chen K, Bandy D, Minoshima S, Thibodeau SN, Osborne D (1996) Preclinical evidence of Alzheimer’s disease in persons homozygous for the epsilon 4 allele for apolipoprotein E. N Engl J Med 334(12):752–758PubMedCrossRefGoogle Scholar
  64. Riekkinen P Jr, Soininen H, Partanen J, Paakkonen A, Helisalmi S, Riekkinen P Sr (1997) The ability of THA treatment to increase cortical alpha waves is related to apolipoprotein E genotype of Alzheimer disease patients. Psychopharmacology 129(3):285–288PubMedCrossRefGoogle Scholar
  65. Rihs TA, Michel CM, Thut G (2007) Mechanisms of selective inhibition in visual spatial attention are indexed by alpha-band EEG synchronization. Eur J Neurosci 25(2):603–610PubMedCrossRefGoogle Scholar
  66. Rodriguez-Valdes R, Manrique-Suarez V, Alvarez-Amador A, Galan-Garcia L, Fernandez-Garcia Y, Lopez-Canovas L, Riveron AM, Bobes-Leon MA (2008) Spectral analysis of the electroencephalogram in subjects with mild cognitive impairment. Rev Neurol 46(5):267–272PubMedGoogle Scholar
  67. Sadato N, Nakamura S, Oohashi T, Nishina E, Fuwamoto Y, Waki A, Yonekura Y (1998) Neural networks for generation and suppression of alpha rhythm: a PET study. Neuroreport 9(5):893–897PubMedCrossRefGoogle Scholar
  68. Saunders AM, Strittmatter WJ, Schmechel D, George-Hyslop PH, Pericak-Vance MA, Joo SH, Rosi BL, Gusella JF, Crapper-MacLachlan DR, Alberts MJ et al (1993) Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer’s disease. Neurology 43(8):1467–1472PubMedCrossRefGoogle Scholar
  69. Sauseng P, Klimesch W, Gruber WR, Birbaumer N (2008) Cross-frequency phase synchronization: a brain mechanism of memory matching and attention. Neuroimage 40(1):308–317PubMedCrossRefGoogle Scholar
  70. Scheeringa R, Bastiaansen MC, Petersson KM, Oostenveld R, Norris DG, Hagoort P (2008) Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int J Psychophysiol 67(3):242–251PubMedCrossRefGoogle Scholar
  71. Schuff N, Woerner N, Boreta L, Kornfield T, Shaw LM, Trojanowski JQ, Thompson PM, Jack CR Jr, Weiner MW (2009) MRI of hippocampal volume loss in early Alzheimer’s disease in relation to ApoE genotype and biomarkers. Brain 132(Pt 4):1067–1077PubMedGoogle Scholar
  72. Schultz MR, Lyons MJ, Franz CE, Grant MD, Boake C, Jacobson KC, Xian H, Schellenberg GD, Eisen SA, Kremen WS (2008) Apolipoprotein E genotype and memory in the sixth decade of life. Neurology 70(19 Pt 2):1771–1777PubMedGoogle Scholar
  73. Shaw P, Lerch JP, Pruessner JC, Taylor KN, Rose AB, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN (2007) Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study. Lancet Neurol 6(6):494–500PubMedCrossRefGoogle Scholar
  74. Shi J, Zhao CB, Vollmer TL, Tyry TM, Kuniyoshi SM (2008) APOE epsilon 4 allele is associated with cognitive impairment in patients with multiple sclerosis. Neurology 70(3):185–190PubMedCrossRefGoogle Scholar
  75. Shulman GL, Pope DL, Astafiev SV, McAvoy MP, Snyder AZ, Corbetta M (2010) Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network. J Neurosci 30(10):3640–3651PubMedCrossRefGoogle Scholar
  76. Skudlarski P, Jagannathan K, Calhoun VD, Hampson M, Skudlarska BA, Pearlson G (2008) Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43(3):554–561PubMedCrossRefGoogle Scholar
  77. Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci USA 95(20):12061–12068PubMedCrossRefGoogle Scholar
  78. Stomrud E, Hansson O, Minthon L, Blennow K, Rosen I, Londos E (2010) Slowing of EEG correlates with CSF biomarkers and reduced cognitive speed in elderly with normal cognition over 4 years. Neurobiol Aging 31(2):215–223PubMedCrossRefGoogle Scholar
  79. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90(5):1977–1981PubMedCrossRefGoogle Scholar
  80. Teipel SJ, Bokde AL, Meindl T, Amaro E Jr, Soldner J, Reiser MF, Herpertz SC, Moller HJ, Hampel H (2010) White matter microstructure underlying default mode network connectivity in the human brain. Neuroimage 49(3):2021–2032PubMedCrossRefGoogle Scholar
  81. Thomann PA, Roth AS, Dos Santos V, Toro P, Essig M, Schroder J (2008) Apolipoprotein E polymorphism and brain morphology in mild cognitive impairment. Dement Geriatr Cogn Disord 26(4):300–305PubMedCrossRefGoogle Scholar
  82. Tomasi D, Volkow ND (2011) Laterality patterns of brain functional connectivity: gender effects. Cereb Cortex. doi:10.1093/cercor/bhr230 Google Scholar
  83. Tu JL, Zhao CB, Vollmer T, Coons S, Lin HJ, Marsh S, Treiman DM, Shi J (2009) APOE 4 polymorphism results in early cognitive deficits in an EAE model. Biochem Biophys Res Commun 384(4):466–470PubMedCrossRefGoogle Scholar
  84. Vazquez Marrufo M, Vaquero E, Cardoso MJ, Gomez CM (2001) Temporal evolution of alpha and beta bands during visual spatial attention. Brain Res Cogn Brain Res 12(2):315–320PubMedCrossRefGoogle Scholar
  85. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81(4):893–926PubMedCrossRefGoogle Scholar
  86. Vogel SA (1990) Gender differences in intelligence, language, visual–motor abilities, and academic achievement in students with learning disabilities: a review of the literature. J Learn Disabil 23(1):44–52PubMedCrossRefGoogle Scholar
  87. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3(4):255–274PubMedCrossRefGoogle Scholar
  88. Wenham PR, Price WH, Blandell G (1991) Apolipoprotein E genotyping by one-stage PCR. Lancet 337(8750):1158–1159PubMedCrossRefGoogle Scholar
  89. Yaffe K, Cauley J, Sands L, Browner W (1997) Apolipoprotein E phenotype and cognitive decline in a prospective study of elderly community women. Arch Neurol 54(9):1110–1114PubMedCrossRefGoogle Scholar
  90. Zitzmann M, Weckesser M, Schober O, Nieschlag E (2001) Changes in cerebral glucose metabolism and visuospatial capability in hypogonadal males under testosterone substitution therapy. Exp Clin Endocrinol Diabetes 109(5):302–304PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Tien-Wen Lee
    • 1
    • 2
  • Younger W.-Y. Yu
    • 3
  • Chen-Jee Hong
    • 4
    • 5
  • Shih-Jen Tsai
    • 4
    • 5
  • Hung-Chi Wu
    • 6
  • Tai-Jui Chen
    • 7
    • 8
  1. 1.Department of PsychiatryChang Gung Memorial HospitalTaoyuanTaiwan
  2. 2.College of MedicineChang Gung UniversityTaoyuanTaiwan
  3. 3.Yu’s Psychiatric ClinicKaohsiungTaiwan, ROC
  4. 4.Department of PsychiatryTaipei Veterans General HospitalTaipeiTaiwan
  5. 5.School of MedicineNational Yang-Ming UniversityTaipeiTaiwan
  6. 6.Kai-Suan Psychiatric HospitalKaohsiungTaiwan, ROC
  7. 7.Department of PsychiatryE-DA HospitalYen-ChaoTaiwan, ROC
  8. 8.Department of Occupational TherapyI-Shou UniversityKaohsiungTaiwan, ROC

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