Distinct laterality alterations distinguish mild cognitive impairment and Alzheimer's disease from healthy aging: Statistical parametric mapping with high resolution MRI

Human Brain Mapping

Volumn 34, Issue 12, 2013, Pages 3400-3410

  Long, Xiaojing ^a   Zhang, Lijuan ^a   Liao, Weiqi ^a   Jiang, Chunxiang ^a   Qiu, Bensheng ^a  

^a SHENZHEN INSTITUTES OF ADVANCED TECHNOLOGY   (China)

Author keywords

Alzheimer's disease; Healthy aging; Hemispheric asymmetry; High resolution MRI; Human brain mapping; MANCOVA; Mild cognitive impairment; Statistical parametric mapping; Voxel based morphometry

Indexed keywords

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN ASYMMETRY; BRAIN MAPPING; BRAIN REGION; ENTORHINAL CORTEX; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; IMAGE PROCESSING; INFERIOR PARIETAL LOBULE; LIMBIC SYSTEM; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; VOXEL BASED MORPHOMETRY; WHITE MATTER;

ALZHEIMER'S DISEASE; HEALTHY AGING; HEMISPHERIC ASYMMETRY; HIGH-RESOLUTION MRI; HUMAN BRAIN MAPPING; MANCOVA; MILD COGNITIVE IMPAIRMENT; STATISTICAL PARAMETRIC MAPPING; VOXEL-BASED MORPHOMETRY;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MENTAL STATUS SCHEDULE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; YOUNG ADULT;

EID: 84886255781     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22157     Document Type: Article

References (82)

1. Albanese A, Merlo A, Mascitti T, Tornese E, Gomez E, Konopka V, Albanese E (1995): Inversion of the hemispheric laterality of the anterior cingulate gyrus in schizophrenics. Biol Psychiat 38:13-21.
2. Albert M, Moss M (1988):Geriatric Neuropsychology.New York:Guilford Press.
3. Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (2000): Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38:304-312.
4. Annett M (1985):Left, Right, Hand and Brain: The Right Shift Theory.London:Lawrence Erlbaum.
5. Barnes J, Scahill R, Schott J, Frost C, Rossor M, Fox N (2005a): Does Alzheimer's disease affect hippocampal asymmetry? Evidence from a cross-sectional and longitudinal volumetric MRI study. Dement Geriatr Cogn Disord 19:338-344.
6. Barnes L, Wilson R, Bienias J, Schneider J, Evans D, Bennett D (2005b): Sex differences in the clinical manifestations of Alzheimer Disease Pathology. Arch Gen Psychiatry 62:685-691.
7. Beaton A (1997): The relation of planum temporale asymmetry and morphology of the corpus callosum to handedness, gender and dyslexia: a review of the evidence. Brain Lang 60:255-322.
8. Bellis T, Nocol T, Kraus N (2000): Aging affects hemispheric asymmetry in the neural representation of speech sounds. J Neurosci 20:791-797.
9. Bonte F, Harris T, Hynan L, Bigio E, White C (2006): Tc-99m HMPAO SPECT in the differential diagnosis of the dementias with histopathologic confirmation. Clin Nucl Med 31( 7):376-378.
10. Broca P (1861): Remarques sur le siège de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole)Bull Soc Anthropol 6:330-357.
11. Brown J, Jaffe J (1975): Hypothesis on cerebral dominance. Neuropsychologia 13:107-110.
12. Cabeza R (2002): Hemispheric asymmetry reduction in old adults: The HAROLD model. Psychol Aging 17:85-100.
13. Cabeza R, Daselaar S, Dolcos F, Prince S, Budde M, Nyberg L (2004): Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb Cortex 14:364-375.
14. Cherbuin N, Reglade-Meslin C, Kumar R, Sachdev P, Anstey K (2010): Mild cognitive disorders are associated with different patterns of brain asymmetry than normal aging: the PATH through life study. Frontiers in psychiatry 1.
15. Coffey C, Lucke J, Saxton J, Ratcliff G, Unitas L, Billig B, Bryan R (1998): Sex differences in brain aging: a quantitative magnetic resonance imaging study. Arch Neurol 55(2):169-179.
16. Coghill R, Gilron I, Iadarola M (2001): Hemispheric lateralization of somatosensory processing. J Neurophysiology 85:2602-2612.
17. Colla M, Ende G, Bohrer M, Deuschle M, Kronenberg G, Henn F, Heuser L (2003): MR spectroscopy in Alzheimer's disease: gender differences in probabilistic learning capacity. Neurobio Aging 24:545-552.
18. Crespo-Facorro B, Roiz-Santianez R, Perez-Iglesias R, Mata I, Rodriguez-Sanchez J, Tordesillas-Gutierrez D, de la Foz V, Tabares-Seisdedos R, Sanchez E, Andreasen N, Magnotta V, Vazquez-Barquero JL (2011): Sex-specific variation of MRI-based cortical morphometry in adult healthy volunteers: The effect on cognitive functioning. Prog Neuropsychopharmacol Biol Psychiatry 35:616-623.
19. Dale A, Sereno M (1993): Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162-176.
20. Dale A, Fischl B, Sereno M (1999): Cortical surface-based analysis i: Segmentation and surface reconstruction. NeuroImage 9( 2):179-194.
21. Davatzikos C, Bryan R (2002): Morphometric analysis of cortical sulci using parametric ribbons: A study of the central sulcus. J Comput Assist Tomogr 26:298-307.
22. Davidson R, Hugdahl K (1995):Brain asymmetry.Cambridge, MA:MIT Press.
23. Dennis N, Kim H, Cabeza R (2007): Effects of aging on true and false memory formation: An fMRI study. Neuropsychologia 45:3157-3166.
24. Derflinger S, Sorg C, Gaser C, Myers N, Arsic M, Kurz A, Zimmer C, Wohlschlager A, Muhlau M (2011): Grey-matter atrophy in Alzheimer's disease is asymmetric but not lateralized. J Alzheimer Dis 25:347-357.
25. Desikan R, Segonne F, Fischl B, Quinn B, Dickerson B, Blacker D, Buckner R, Dale A, Maguire R, Hyman B, Albert MS, Killiany RJ (2006): An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968-980.
26. Deslandes A, de Moraes H, Pompeu F, Ribeiro P, Cagy M, Capitao C, Alves H, Piedade R, Laks J. (2008): Electroencephalographic frontal asymmetry and depressive symptoms in the elderly. Biol Psychol 79:317-322.
27. Devanand D, Pradhaban G, Liu X, Khandji A, De Santi S, Segal S, Rusinek H, Pelton G, Honig L, Mayeux R, Stern Y, Tabert MH, de Leon MJ (2007): Hippocampal and entorhinal atrophy in mild cognitive impairment: Prediction of Alzheimer disease. Neurology 68:828-836.
28. Dickerson B (2007): The entorhinal cortex: An anatomical mediator of genetic vulnerability to Alzheimer's disease. Lancet Neurol 6:471-473.
29. Eberstaller O (1884): Zür Oberflachen Anatomie der Grosshirn Hemisphaeren. Wien Med 479:642-644.
30. Fallgatter A, Roesler M, Sitzmann L, Heidrich A, Mueller T, Strik W (1997): Loss of functional hemispheric asymmetry in Alzheimer's dementia assessed with near-infrared spectroscopy. Cogn Brain Res 6:67-72.
31. Fischl B (2012): FreeSurfer. NeuroImage 62:774-781.
32. Fischl B, Dale A (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050-11055.
33. Fischl B, Sereno M, Dale A (1999): Cortical surface-based analysis-ii: Inflation, flatting, and a surface-based coordinate system. Neuroimage 9:195-207.
34. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat D, Busa E, Seidman L, Goldstein J, Kennedy D, Carviness V, Makris N, Rosen B, Dale A (2004): Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11-22.
35. Folstein M, Folstein S, McHugh P (1975): Mini-mental state: A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198.
36. Gannon P, Kheck N, Braun A, Ralph L, Holloway R (2005): Planum parietale of chimpanzees and orangutans: A comparative resonance of human-like planum temporale asymmetry. Anat Rec A Discov Mol Cell Evol Biol 287:1128-1141.
37. Geshwind D, Lacobini M (1999):Structural and functional asymmetries of the frontal lobes.New York:Guilford Publications.
38. Good C, Johnsrude I, Ashburner J, Henson R, Friston K, Frackowiak R (2001): Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage 14:685-700.
39. Han X, Jovichich J, Salat D, van der Kouwe A, Quinn B, Czanner S, Busa E, Pacheco J, Albert M, Killiany R, Maguire P, Rosas D, Makris N, Dale A (2006): Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. NeuroImage 32:180-194.
40. Hausmann M (2005): Hemispheric asymmetry in spatial attention across the menstrual cycle. Neuropsychologia 43:1559-1567.
41. Hellige J (1993):Hemispheric Asymmetry: What's Right and what's Left.Cambridge, MA:Harvard University Press.
42. Herrmann M, Walter A, Ehlis A-C, Fallgatter A (2006): Cerebral oxygenation changes in the prefrontal cortex: Effects of age and gender. Neurobiol Aging 27:888-894.
43. Hugdahl K, Thomsen T, Ersland L (2006): Sex differences in visuo-spatial processing: An fMRI study of mental rotation. Neuropsychologia 44:1575-1583.
44. Hutsler J, Loftus W, Gazzaniga M (1998): Individual variation of cortical surface area asymmetry. Cereb Cortex 8:11-17.
45. Im K, Lee J, Seo S, Kim S, Na D (2008): Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer's disease. Neuroimage 43:103-113.
46. Jack C Jr., Dickson D, Parisi J, Xu Y, Cha R, O'Brien P, Edland S, Smith G, Boeve B, Tangalos E, Kokmen E, Petersen RC (2002): Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 58:750-757.
47. Jorm A, Jolley D. (1998): The incidence of dementia: A meta-analysis. Neurology 51:728-733.
48. Kochunov P, Mangin J, Coyle T, Lancaster J, Thompson P, Rivière D, Cointepas Y, Régis J, Schlosser A, Royall D, Zilles K, Mazziotta J, Toga A, Fox PT (2005): Age-related morphology trends of cortical sulci. Hum Brain Mapp 26:210-220.
49. Kochunov P, Thompson P, Coyle T, Lancaster J, Kochunov V, Royall D, Mangin J, Rivière D, Fox P (2008): Relationship among neuroimaging indices of cerebral healthy during normal aging. Hum Brain Mapp 29:36-45.
50. Lütcke H, Frahm J (2008): Lateralized anterior cingulate function during error processing and conflict monitoring as revealed by high-resolution fMRI. Cereb Cortex 18:508-515.
51. Letenneur L, Gilleron V, Commenges D, Helmer C, Orgogozo J, Dartigues J. (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.
52. Li Z, Moore A, Tyner C, Hu X. (2009): Asymmetric connectivity reduction and its relationship to HAROLD in aging brain. Brain Res 1295:149-158.
53. Liu T, Wen W, Zhu W, Trollor J, Reppermund S, Crawford J, Jin J, Luo S, Brodaty H, Sachdev P (2010): The effects of age and sex on cortical sulci in the elderly. Neuroimage 51:19-27.
54. Liu T, Wen W, Zhu W, Kochan N, Trollor J, Reppermund S, Jin J, Luo S, Brodaty H, Sachdev P (2011): The relationship between cortical sulcal variability and cognitive performance in the elderly. Neuroimage 56:865-873.
55. Luders E, Narr K, Thompson P, Rex D, Jancke L, Toga A (2005): Hemispheric asymmetries in cortical thickness. Cereb Cortex 16:1232-1238.
56. Lyttelton O, Karama S, Ad-Dab'bagh Y, Zatorre R, Carbonell F, Worsley K, Evans A (2009): Positional and surface area asymmetry of the human cerebral cortex. Neuroimage 46:895-903.
57. Morris J (1993): Clinical dementia rating (CDR): Current version and scoring rules. Neurology 43:2412-2414.
58. Oertel V, Knöchel C, Rotarska-Jagiela A, Schönmeyer R, Lindner M, van de Ven V, Haenschel C, Uhlhaas P, Maurer K, Linden D (2010): Reduced laterality as a trait marker of schizophrenia-Evidence from structural and functional neuroimaging. J Neurosci 30:2289-2299.
59. Ott B, Tate C, Gordon N, Heindel W (1996): Gender differences in the behavioral manifestations of Alzheimer's disease. J Am Geriatr Soc 44:583-587.
60. Ott B, Heindel W, Tan Z, Noto R (2000): Lateralized cortical perfusion in women with Alzheimer's disease. J Gend Specif Med 3:29-35.
61. Penhune V, Zatorre R, MacDonald J, Evans A (1996): Interhemispheric anatomical differences in human primary auditory cortex: Probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6:661-672.
62. Posthuma D, De Geus E, Baaré W, Hulshoff Pol H, Kahn R, Boomsma D (2002): The association between brain volume and intelligence is of genetic origin. Nat Neurosci 5:83-84.
63. Price C (2000): The anatomy of language: Contributions from functional neuroimaging. J Anat 197:335-359.
64. Pujol J, Lopez A, Deus J, Cardoner N, Vallejo J (2002): Anatomical variability of the anterior cingulate gyrus and basic dimensions of human personality. Neuroimage 15:847-855.
65. Reuter-Lorenz P, Stanczak L, Miller A (1999): Neural recruitment and cognitive aging: Two hemispheres are better than one, especially as you age. Psychol Sci 10:494-500.
66. Ripich D, Petrill S, Whitehouse P, Ziol E (1995): Gender differences in language of AD patients: A longitudinal study. Neurology 45:299-302.
67. Rogers L (2002):Advantages and Disadvantages of Lateralization.Cambridge:Cambridge University Press.
68. Schaer M, Bach Cuadra M, Tamarit L, Lazeyras F, Eliez S, Thiran J (2008): A surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 27:161-170.
69. Schroeter M, Stein T, Maslowski N, Neumann J (2009): Neural correlates of Alzheimer's disease and mild cognitive impairment: A systematic and quantitative meta-analysis involving 1, 351 patients. Neuroimage 47:1196-1206.
70. Shi F, Liu B, Zhou Y, Yu C, Jiang T (2009): Hippocampal volume and asymmetry in mild cognitive impairment and Alzheimer's disease: Metaanalyses of MRI studies. Hippocampus 19:1055-1064.
71. Sowell E, Peterson B, Thompson P, Welcome S, Henkenius A, Toga A (2003): Mapping cortical change across the human life span. Nat Neurosci 6:309-315.
72. Steinmetz H (1996): Structure, functional and cerebral asymmetry: In vivo morphometry of the planum temporale. Neurosci Biobehav Rev 20:587-591.
73. Seo SW, Lee JH, Jang SM, Kim ST, Chin J, Kim GH, Kim JH, Roh JH, Kim MJ, Kim SH, Na DL (2012): Neurochemical alterations of the entorhinal cortex in amnestic mild cognitive impairment (aMCI): a three-year follow-up study. Arch Gerontol Geriatr 54:192-196.
74. Thompson P, Cannon T, Narr K, van Erp T, Poutanen V, Huttunen M, Lönnqvist J, Standertskjöld-Nordenstam C, Kaprio J, Khaledy M, Dail R, Zoumalan CI, Toga AW (2001): Genetic influences on brain structure. Nat Neurosci 4:1253-1258.
75. Thompson P, Hayashi K, de Zubicaray G, Janke A, Rose S, Semple J, Herman D, Hong M, Dittmer S, Doddrell D, Toga AW (2003): Dynamics of gray matter loss in Alzheimer's disease. J Neurosci 23:994-1005.
76. Thompson P, Hayashi K, Dutton R, Chiang M, Leow A, Sowell E, De Zubicaray G, Becker J, Lopez O, Aizenstein H, Toga AW (2007): Tracking Alzheimer's disease. Ann NY Acad Sci 1097:183-214.
77. Tomasi D, Volkow ND (2012): Laterality patterns of brain functional connectivity: gender effects. Cereb Cortex 22:1455-1462.
78. van der Flier W, Pijenburg Y, Fox N, Scheltens P. (2011): Early-onset versus later onset Alzheimer's disease: The case of the missing APOE 4 allele. Lancet Neurol 3:280-288.
79. Voyer D. (1996): On the magnitude of laterality effects and sex differences in functional lateralities. Laterality 1:51-83.
80. Watkins K, Paus T, Lerch J, Zijdenbos A, Collins D, Neelin P, Taylor J, Worsley K, Evans A. (2001): Structural asymmetries in the human brain: A voxel-based statistical analysis of 142 MRI scans. Cereb Cortex 11:868-877.
81. Wernicke C (1874):Der aphasische Symptomencomplex: eine psychologische Studie auf anatomischer Basis.Breslau:Cohn und Welgert.
82. Zhong J, Phua D, Qiu A (2010): Quantitative evaluation of LDDMM, FreeSurfer and CARET for cortical surface mapping. Neuroimage 52:131-141.