Dement Neurocogn Disord.  2019 Sep;18(3):77-95. 10.12779/dnd.2019.18.3.77.

The Cortical Neuroanatomy Related to Specific Neuropsychological Deficits in Alzheimer's Continuum

• Kang SH
• Park YH
• Lee D
• Kim JP
• Chin J
• Ahn Y
• Park SB
• Kim HJ
• Jang H
• Jung YH
• Kim J
• Lee J
• Kim JS
• Cheon BK
• Hahn A
• Lee H
• Na DL
• Kim YJ
• Seo SW

• KMID: 2461049
• DOI: http://doi.org/10.12779/dnd.2019.18.3.77

Abstract

BACKGROUND AND PURPOSE
In Alzheimer's continuum (a comprehensive of preclinical Alzheimer's disease [AD], mild cognitive impairment [MCI] due to AD, and AD dementia), cognitive dysfunctions are often related to cortical atrophy in specific brain regions. The purpose of this study was to investigate the association between anatomical pattern of cortical atrophy and specific neuropsychological deficits.
METHODS
A total of 249 participants with Alzheimer's continuum (125 AD dementia, 103 MCI due to AD, and 21 preclinical AD) who were confirmed to be positive for amyloid deposits were collected from the memory disorder clinic in the department of neurology at Samsung Medical Center in Korea between September 2013 and March 2018. To analyze neuropsychological test-specific neural correlates representing the relationship between cortical atrophy measured by cortical thickness and performance in specific neuropsychological tests, a linear regression analysis was performed. Two neural correlates acquired by 2 different standardized scores in neuropsychological tests were also compared.
RESULTS
Cortical atrophy in several specific brain regions was associated with most neuropsychological deficits, including digit span backward, naming, drawing-copying, verbal and visual recall, semantic fluency, phonemic fluency, and response inhibition. There were a few differences between 2 neural correlates obtained by different z-scores.
CONCLUSIONS
The poor performance of most neuropsychological tests is closely related to cortical thinning in specific brain areas in Alzheimer's continuum. Therefore, the brain atrophy pattern in patients with Alzheimer's continuum can be predict by an accurate analysis of neuropsychological tests in clinical practice.

Keyword

Neuropsychological Tests; Cortical Atrophy; Alzheimer's Disease; Alzheimer's Continuum; Cognition; Neural Correlates

MeSH Terms

Alzheimer Disease
Atrophy
Brain
Cognition
Dementia
Humans
Korea
Linear Models
Memory Disorders
Mild Cognitive Impairment
Neuroanatomy*
Neurology
Neuropsychological Tests
Plaque, Amyloid
Semantics

Figure

• 

  Fig. 1 Correlation maps demonstrating associations between cortical thickness and neuropsychological tests in patients with Alzheimer's continuum (AI >0 means right-sided correlated areas > left-sided correlated areas, and vice versa for AI <0). AI: asymmetric index, BNT: Boston Naming Test, SVLT: Seoul Verbal Learning Test, RCFT: Rey-Osterrieth Complex Figure Test, COWAT: Controlled Oral Word Association Test, DSC: Digit Symbol Coding, CDT: Clock Drawing Test.

• 

  Fig. 2 Difference in cortical atrophy pattern between correlation maps with SNSB-II z-score and those with SNSB-I z-score. BNT: Boston Naming Test, SVLT: Seoul Verbal Learning Test, RCFT: Rey-Osterrieth Complex Figure Test, COWAT: Controlled Oral Word Association Test, SNSB: Seoul Neuropsychological Screening Battery, SMA: supplementary motor area.

Reference

1. MacPherson SE, Cox SR, Dickie DA, Karama S, Starr JM, Evans AC, et al. Processing speed and the relationship between Trail Making Test-B performance, cortical thinning and white matter microstructure in older adults. Cortex. 2017; 95:92–103.

2. Vallesi A, Mazzonetto I, Ambrosini E, Babcock L, Capizzi M, Arbula S, et al. Structural hemispheric asymmetries underlie verbal Stroop performance. Behav Brain Res. 2017; 335:167–173.

3. Zink DN, Miller JB, Caldwell JZ, Bird C, Banks SJ. The relationship between neuropsychological tests of visuospatial function and lobar cortical thickness. J Clin Exp Neuropsychol. 2018; 40:518–527.

4. Ahn HJ, Seo SW, Chin J, Suh MK, Lee BH, Kim ST, et al. The cortical neuroanatomy of neuropsychological deficits in mild cognitive impairment and Alzheimer's disease: a surface-based morphometric analysis. Neuropsychologia. 2011; 49:3931–3945.

5. Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, et al. NIA-AA research framework: toward a biological definition of Alzheimer's disease. Alzheimers Dement. 2018; 14:535–562.

6. Kang YJ, Na DL. Seoul Neuropsychological Screening Battery (SNSB-II). 2nd ed. Seoul: Human Brain Research & Consulting Co.;2012.

7. Flynn JR. The mean IQ of Americans: massive gains 1932 to 1978. Psychol Bull. 1984; 95:29–51.

8. Wechsler D. Wechsler Intelligence Scale for Children-Revised. New York: Psychological Corporation;1974.

9. Wechsler D. Wechsler Adult Intelligence Scale-Revised. New York: Psychological Corporation;1981.

10. Wechsler D. Wechsler Adult Intelligence Scale-III. New York: Psychological Corporation;1997.

11. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, et al. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011; 7:280–292.

12. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment 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; 7:270–279.

13. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, 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; 7:263–269.

14. Zijdenbos AP, Forghani R, Evans AC. Automatic “pipeline” analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans Med Imaging. 2002; 21:1280–1291.

15. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr. 1994; 18:192–205.

16. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 1998; 17:87–97.

17. Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab'bagh Y, MacDonald D, et al. Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage. 2005; 27:210–221.

18. MacDonald D, Kabani N, Avis D, Evans AC. Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage. 2000; 12:340–356.

19. Lerch JP, Evans AC. Cortical thickness analysis examined through power analysis and a population simulation. Neuroimage. 2005; 24:163–173.

20. Im K, Lee JM, Lyttelton O, Kim SH, Evans AC, Kim SI. Brain size and cortical structure in the adult human brain. Cereb Cortex. 2008; 18:2181–2191.

21. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002; 17:143–155.

22. Im K, Lee JM, Lee J, Shin YW, Kim IY, Kwon JS, et al. Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage. 2006; 31:31–38.

23. Lyttelton O, Boucher M, Robbins S, Evans A. An unbiased iterative group registration template for cortical surface analysis. Neuroimage. 2007; 34:1535–1544.

24. Chung MK, Worsley KJ, Robbins S, Paus T, Taylor J, Giedd JN, et al. Deformation-based surface morphometry applied to gray matter deformation. Neuroimage. 2003; 18:198–213.

25. Shimamura AP, Janowsky JS, Squire LR. Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients. Neuropsychologia. 1990; 28:803–813.

26. McAndrews MP, Milner B. The frontal cortex and memory for temporal order. Neuropsychologia. 1991; 29:849–859.

27. Chiba AA, Kesner RP, Reynolds AM. Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. Behav Neural Biol. 1994; 61:123–131.

28. Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L. Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J Cogn Neurosci. 2000; 12:197–206.

29. Cabeza R, Mangels J, Nyberg L, Habib R, Houle S, McIntosh AR, et al. Brain regions differentially involved in remembering what and when: a PET study. Neuron. 1997; 19:863–870.

30. Majerus S, D'Argembeau A, Martinez Perez T, Belayachi S, Van der Linden M, Collette F, et al. The commonality of neural networks for verbal and visual short-term memory. J Cogn Neurosci. 2010; 22:2570–2593.

31. Jenkins LJ, Ranganath C. Prefrontal and medial temporal lobe activity at encoding predicts temporal context memory. J Neurosci. 2010; 30:15558–15565.

32. Tubridy S, Davachi L. Medial temporal lobe contributions to episodic sequence encoding. Cereb Cortex. 2011; 21:272–280.

33. Marshuetz C, Smith EE. Working memory for order information: multiple cognitive and neural mechanisms. Neuroscience. 2006; 139:195–200.

34. Marshuetz C, Smith EE, Jonides J, DeGutis J, Chenevert TL. Order information in working memory: fMRI evidence for parietal and prefrontal mechanisms. J Cogn Neurosci. 2000; 12:Suppl 2. 130–144.

35. Canavan AG, Passingham RE, Marsden CD, Quinn N, Wyke M, Polkey CE. Sequence ability in parkinsonians, patients with frontal lobe lesions and patients who have undergone unilateral temporal lobectomies. Neuropsychologia. 1989; 27:787–798.

36. Gerton BK, Brown TT, Meyer-Lindenberg A, Kohn P, Holt JL, Olsen RK, et al. Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging. Neuropsychologia. 2004; 42:1781–1787.

37. Hoshi Y, Oda I, Wada Y, Ito Y, Yamashita Y, Oda M, et al. Visuospatial imagery is a fruitful strategy for the digit span backward task: a study with near-infrared optical tomography. Brain Res Cogn Brain Res. 2000; 9:339–342.

38. Bookheimer S. Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu Rev Neurosci. 2002; 25:151–188.

39. Apostolova LG, Lu P, Rogers S, Dutton RA, Hayashi KM, Toga AW, et al. 3D mapping of language networks in clinical and pre-clinical Alzheimer's disease. Brain Lang. 2008; 104:33–41.

40. Baldo JV, Arévalo A, Patterson JP, Dronkers NF. Grey and white matter correlates of picture naming: evidence from a voxel-based lesion analysis of the Boston Naming Test. Cortex. 2013; 49:658–667.

41. Lau JK, Humphreys GW, Douis H, Balani A, Bickerton WL, Rotshtein P. The relation of object naming and other visual speech production tasks: a large scale voxel-based morphometric study. Neuroimage Clin. 2015; 7:463–475.

42. Biesbroek JM, van Zandvoort MJ, Kuijf HJ, Weaver NA, Kappelle LJ, Vos PC, et al. The anatomy of visuospatial construction revealed by lesion-symptom mapping. Neuropsychologia. 2014; 62:68–76.

43. Tranel D, Rudrauf D, Vianna EP, Damasio H. Does the Clock Drawing Test have focal neuroanatomical correlates? Neuropsychology. 2008; 22:553–562.

44. Matsuoka T, Narumoto J, Okamura A, Taniguchi S, Kato Y, Shibata K, et al. Neural correlates of the components of the clock drawing test. Int Psychogeriatr. 2013; 25:1317–1323.

45. Hirjak D, Wolf RC, Pfeifer B, Kubera KM, Thomann AK, Seidl U, et al. Cortical signature of clock drawing performance in Alzheimer's disease and mild cognitive impairment. J Psychiatr Res. 2017; 90:133–142.

46. Teipel SJ, Willoch F, Ishii K, Bürger K, Drzezga A, Engel R, et al. Resting state glucose utilization and the CERAD cognitive battery in patients with Alzheimer's disease. Neurobiol Aging. 2006; 27:681–690.

47. Becker JT, Mintun MA, Aleva K, Wiseman MB, Nichols T, DeKosky ST. Compensatory reallocation of brain resources supporting verbal episodic memory in Alzheimer's disease. Neurology. 1996; 46:692–700.

48. Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S. Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci U S A. 1994; 91:2016–2020.

49. Baddeley A. The central executive: a concept and some misconceptions. J Int Neuropsychol Soc. 1998; 4:523–526.

50. Squire LR, Wixted JT. The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci. 2011; 34:259–288.

51. Jeong SK, Xu Y. Task-context-dependent linear representation of multiple visual objects in human parietal cortex. J Cogn Neurosci. 2017; 29:1778–1789.

52. Kravitz DJ, Saleem KS, Baker CI, Mishkin M. A new neural framework for visuospatial processing. Nat Rev Neurosci. 2011; 12:217–230.

53. Ungerleider LG, Haxby JV. ‘What’ and ‘where’ in the human brain. Curr Opin Neurobiol. 1994; 4:157–165.

54. Lam LC, Ho P, Lui VW, Tam CW. Reduced semantic fluency as an additional screening tool for subjects with questionable dementia. Dement Geriatr Cogn Disord. 2006; 22:159–164.

55. Perret E. The left frontal lobe of man and the suppression of habitual responses in verbal categorical behaviour. Neuropsychologia. 1974; 12:323–330.

56. Henry JD, Crawford JR. A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology. 2004; 18:284–295.

57. MacLeod CM. Half a century of research on the Stroop effect: an integrative review. Psychol Bull. 1991; 109:163–203.

58. Cieslik EC, Mueller VI, Eickhoff CR, Langner R, Eickhoff SB. Three key regions for supervisory attentional control: evidence from neuroimaging meta-analyses. Neurosci Biobehav Rev. 2015; 48:22–34.

59. Laird AR, McMillan KM, Lancaster JL, Kochunov P, Turkeltaub PE, Pardo JV, et al. A comparison of label-based review and ALE meta-analysis in the Stroop task. Hum Brain Mapp. 2005; 25:6–21.

60. Cipolotti L, Spanò B, Healy C, Tudor-Sfetea C, Chan E, White M, et al. Inhibition processes are dissociable and lateralized in human prefrontal cortex. Neuropsychologia. 2016; 93:1–12.

61. Vasconcelos LG, Jackowski AP, Oliveira MO, Flor YM, Souza AA, Bueno OF, et al. The thickness of posterior cortical areas is related to executive dysfunction in Alzheimer's disease. Clinics (Sao Paulo). 2014; 69:28–37.

62. Wolk DA, Dickerson BC. Alzheimer's Disease Neuroimaging Initiative. Apolipoprotein E (APOE) genotype has dissociable effects on memory and attentional-executive network function in Alzheimer's disease. Proc Natl Acad Sci U S A. 2010; 107:10256–10261.

63. Dickerson BC, Wolk DA. Alzheimer's Disease Neuroimaging Initiative. Dysexecutive versus amnesic phenotypes of very mild Alzheimer's disease are associated with distinct clinical, genetic and cortical thinning characteristics. J Neurol Neurosurg Psychiatry. 2011; 82:45–51.

64. Birn RM, Kenworthy L, Case L, Caravella R, Jones TB, Bandettini PA, et al. Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage. 2010; 49:1099–1107.

65. Mummery CJ, Patterson K, Hodges JR, Wise RJ. Generating ‘tiger’ as an animal name or a word beginning with T: differences in brain activation. Proc Biol Sci. 1996; 263:989–995.

66. Mull BR, Seyal M. Transcranial magnetic stimulation of left prefrontal cortex impairs working memory. Clin Neurophysiol. 2001; 112:1672–1675.

67. Lezak MD, Loring DW. Neuropsychological Assessment. 5th ed. Oxford: Oxford University Press;2012.

68. Cahn-Weiner DA, Sullivan EV, Shear PK, Fama R, Lim KO, Yesavage JA, et al. Brain structural and cognitive correlates of clock drawing performance in Alzheimer's disease. J Int Neuropsychol Soc. 1999; 5:502–509.

69. Lee DY, Seo EH, Choo IH, Kim SG, Lee JS, Lee DS, et al. Neural correlates of the Clock Drawing Test performance in Alzheimer's disease: a FDG-PET study. Dement Geriatr Cogn Disord. 2008; 26:306–313.

70. Nagahama Y, Okina T, Suzuki N, Nabatame H, Matsuda M. Neural correlates of impaired performance on the clock drawing test in Alzheimer's disease. Dement Geriatr Cogn Disord. 2005; 19:390–396.

71. Ueda H, Kitabayashi Y, Narumoto J, Nakamura K, Kita H, Kishikawa Y, et al. Relationship between clock drawing test performance and regional cerebral blood flow in Alzheimer's disease: a single photon emission computed tomography study. Psychiatry Clin Neurosci. 2002; 56:25–29.

72. Makuuchi M, Kaminaga T, Sugishita M. Both parietal lobes are involved in drawing: a functional MRI study and implications for constructional apraxia. Brain Res Cogn Brain Res. 2003; 16:338–347.

73. Milner B. Biology of Memory. New York: Academic Press;1970. p. 29–50.

74. Kelley WM, Miezin FM, McDermott KB, Buckner RL, Raichle ME, Cohen NJ, et al. Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding. Neuron. 1998; 20:927–936.