Default Mode Network Connectivity and Related White Matter Disruption in Type 2 Diabetes Mellitus Patients Concurrent with Amnestic Mild Cognitive Impairment

Page: [1238 - 1246] Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Background: As a risk factor for Alzheimer's disease (AD), type 2 diabetes mellitus (T2DM) itself causes cognitive impairment and has higher prevalence of mild cognitive impairment (MCI). Objective: The aim of this study was to explore the cognition especially the episodic memory difference, the DMN functional connectivity and DMN-related white matter integrity in patients with both T2DM and amnestic MCI (T2DM-MCI) as compared to patients with T2DM only.

Methods: Focusing especially on T2DM population, we investigated the default mode network (DMN) through resting-state functional magnetic resonance imaging among 22 elderly T2DM-MCI patients and 24 elderly T2DM patients. Including primarily the bilateral cingulum, hippocampus and uncinate fasciculus, these DMN white matter fibers were also closely associated with episodic memory and the integrity of them was also investigated using diffusion tensor imaging in 19 elderly T2DM-MCI patients and 23 elderly T2DM patients.

Results: Compared with the patients with T2DM, the T2DM-MCI patients performed worse in several areas of cognition besides episodic memory, and showed stronger DMN functional connectivity in the left precuneus and weaker functional connectivity in the left calcarine, as well as decreased integrity of the left cingulate bundle and bilateral uncinate fasciculus. Furthermore, a correlation analysis indicated that higher left calcarine connectivity was associated with better episodic memory performance among the overall group.

Conclusion: Our results demonstrated that T2DM patients with comorbid amnestic MCI had abnormal functional connectivity patterns and decreased white matter integrity, which could potentially serve as AD or AD risk biomarkers for early detection of those elderly individuals with T2DM.

Keywords: Type 2 diabetes mellitus, mild cognitive impairment, episodic memory, default mode network, functional connectivity, white matter integrity.

[1]
Cheng G, Huang C, Deng H, Wang H. Diabetes as a risk factor for dementia and mild cognitive impairment: a meta-analysis of longitudinal studies. Intern Med J 42(5): 484-91. (2012).
[2]
Toro P, Schonknecht P, Schroder J. Type II diabetes in mild cognitive impairment and Alzheimer’s disease: results from a prospective population-based study in Germany. J Alzheimers Dis 16(4): 687-91. (2009).
[3]
Morris JK, Vidoni ED, Honea RA, Burns JM. Alzheimer’s Disease Neuroimaging I. Impaired glycemia increases disease progression in mild cognitive impairment. Neurobiol Aging 35(3): 585-9. (2014).
[4]
Li J, Wang YJ, Zhang M, Xu ZQ, Gao CY, Fang CQ, et al. Vascular risk factors promote conversion from mild cognitive impairment to Alzheimer disease. Neurology 76(17): 1485-91. (2011).
[5]
Ma F, Wu T, Miao R, Xiao YY, Zhang W, Huang G. Conversion of mild cognitive impairment to dementia among subjects with diabetes: a population-based study of incidence and risk factors with five years of follow-up. J Alzheimers Dis 43(4): 1441-9. (2015).
[6]
Dubois B, Albert ML. Amnestic MCI or prodromal Alzheimer’s disease? Lancet Neurol 3(4): 246-8. (2004).
[7]
Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56(3): 303-8. (1999).
[8]
Strachan MW, Deary IJ, Ewing FM, Frier BM. Is type II diabetes associated with an increased risk of cognitive dysfunction? A critical review of published studies. Diabetes Care 20(3): 438-45. (1997).
[9]
Grober E, Hall CB, Hahn SR, Lipton RB. Memory impairment and executive dysfunction are associated with inadequately controlled diabetes in older adults. J Prim Care Community Health 2(4): 229-33. (2011).
[10]
Mehrabian S, Raycheva M, Gateva A, Todorova G, Angelova P, Traykova M, et al. Cognitive dysfunction profile and arterial stiffness in type 2 diabetes. J Neurol Sci 322(1-2): 152-6. (2012).
[11]
Sestieri C, Corbetta M, Romani GL, Shulman GL. Episodic memory retrieval, parietal cortex, and the default mode network: functional and topographic analyses. J Neurosci 31(12): 4407-20. (2011).
[12]
Jeong W, Chung CK, Kim JS. Episodic memory in aspects of large-scale brain networks. Front Hum Neurosci 9: 454. (2015).
[13]
Buckner RL, Andrews-Hanna JR, Schacter DL. The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124: 1-38. (2008).
[14]
Dickerson BC. Advances in functional magnetic resonance imaging: technology and clinical applications. Neurotherapeutics 4(3): 360-70. (2007).
[15]
Greicius MD, Srivastava G, Reiss AL, Menon V. Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101(13): 4637-42. (2004).
[16]
Rombouts SA, Barkhof F, Goekoop R, Stam CJ, Scheltens P. Altered resting state networks in mild cognitive impairment and mild Alzheimer’s disease: an fMRI study. Hum Brain Mapp 26(4): 231-9. (2005).
[17]
Musen G, Jacobson AM, Bolo NR, Simonson DC, Shenton ME, McCartney RL, et al. Resting-state brain functional connectivity is altered in type 2 diabetes. Diabetes 61(9): 2375-9. (2012).
[18]
Marder TJ, Flores VL, Bolo NR, Hoogenboom WS, Simonson DC, Jacobson AM, et al. Task-induced brain activity patterns in type 2 diabetes: a potential biomarker for cognitive decline. Diabetes 63(9): 3112-9. (2014).
[19]
Hagmann P, Thiran JP, Jonasson L, Vandergheynst P, Clarke S, Maeder P, et al. DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection. Neuroimage 19(3): 545-54. (2003).
[20]
Simons JS, Spiers HJ. Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4(8): 637-48. (2003).
[21]
Teipel SJ, Bokde AL, Meindl T, Amaro E Jr, Soldner J, Reiser MF, et al. White matter microstructure underlying default mode network connectivity in the human brain. NeuroImage 49(3): 2021-32. (2010).
[22]
Kiuchi K, Morikawa M, Taoka T, Nagashima T, Yamauchi T, Makinodan M, et al. Abnormalities of the uncinate fasciculus and posterior cingulate fasciculus in mild cognitive impairment and early Alzheimer’s disease: a diffusion tensor tractography study. Brain Res 1287: 184-91. (2009).
[23]
Hsu JL, Chen YL, Leu JG, Jaw FS, Lee CH, Tsai YF, et al. Microstructural white matter abnormalities in type 2 diabetes mellitus: a diffusion tensor imaging study. NeuroImage 59(2): 1098-105. (2012).
[24]
Ma F, Wu T, Miao R, Xiao YY, Zhang W, Huang G. Conversion of mild cognitive impairment to dementia among subjects with diabetes: a population-based study of incidence and risk factors with five years of follow-up. J Alzheimers Dis 43(4): 1441-9. (2015).
[25]
Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med 256(3): 183-94. (2004).
[26]
Zhang M, Elena Y, He Y. Activities of daily living scale. Shanghai Arch Psychiatry 7: 3. (1995).
[27]
Chen Y, Liu Z, Zhang J, Xu K, Zhang S, Wei D, et al. Altered brain activation patterns under different working memory loads in patients with type 2 diabetes. Diabetes Care 37(12): 3157-63. (2014).
[28]
Chen Y, Wang J, Zhang J, Zhang T, Chen K, Fleisher A, et al. Aberrant functional networks connectivity and structural atrophy in silent lacunar infarcts: relationship with cognitive impairments. J Alzheimers Dis 42(3): 841-50. (2014).
[29]
Fellgiebel A, Wille P, Muller MJ, Winterer G, Scheurich A, Vucurevic G, et al. Ultrastructural hippocampal and white matter alterations in mild cognitive impairment: a diffusion tensor imaging study. Dement Geriatr Cogn Disord 18(1): 101-8. (2004).
[30]
Fellgiebel A, Muller MJ, Wille P, Dellani PR, Scheurich A, Schmidt LG, et al. Color-coded diffusion-tensor-imaging of posterior cingulate fiber tracts in mild cognitive impairment. Neurobiol Aging 26(8): 1193-8. (2005).
[31]
Diehl B, Busch RM, Duncan JS, Piao Z, Tkach J, Luders HO. Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia 49(8): 1409-18. (2008).
[32]
Chen Y, Wang A, Tang J, Wei D, Li P, Chen K, et al. Association of white matter integrity and cognitive functions in patients with subcortical silent lacunar infarcts. Stroke 46(4): 1123-6. (2015).
[33]
Brands AM, Van den Berg E, Manschot SM, Biessels GJ, Kappelle LJ, De Haan EH, et al. A detailed profile of cognitive dysfunction and its relation to psychological distress in patients with type 2 diabetes mellitus. J Int Neuropsychol Soc 13(2): 288-97. (2007).
[34]
Zhang J, Wang Y, Wang J, Zhou X, Shu N, Wang Y, et al. White matter integrity disruptions associated with cognitive impairments in type 2 diabetic patients. Diabetes 63(11): 3596-605. (2014).
[35]
Greicius MD, Srivastava G, Reiss AL, Menon V. Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101(13): 4637-42. (2004).
[36]
Zhang HY, Wang SJ, Liu B, Ma ZL, Yang M, Zhang ZJ, et al. Resting brain connectivity: changes during the progress of Alzheimer disease. Radiology 256(2): 598-606. (2010).
[37]
Yi D, Choe YM, Byun MS, Sohn BK, Seo EH, Han J, et al. Differences in functional brain connectivity alterations associated with cerebral amyloid deposition in amnestic mild cognitive impairment. Front Aging Neurosci 7: 15. (2015).
[38]
Agosta F, Pievani M, Geroldi C, Copetti M, Frisoni GB, Filippi M. Resting state fMRI in Alzheimer’s disease: beyond the default mode network. Neurobiol Aging 33(8): 1564-78. (2012).
[39]
Yi L, Wang J, Jia L, Zhao Z, Lu J, Li K, et al. Structural and functional changes in subcortical vascular mild cognitive impairment: a combined voxel-based morphometry and resting-state fMRI study. PloS One 7(9): e44758 (2012).
[40]
Lundstrom BN, Petersson KM, Andersson J, Johansson M, Fransson P, Ingvar M. Isolating the retrieval of imagined pictures during episodic memory: activation of the left precuneus and left prefrontal cortex. NeuroImage 20(4): 1934-43. (2003).
[41]
Sadigh-Eteghad S, Majdi A, Farhoudi M, Talebi M, Mahmoudi J. Different patterns of brain activation in normal aging and Alzheimer’s disease from cognitional sight: meta analysis using activation likelihood estimation. J Neurol Sci 343(1-2): 159-66. (2014).
[42]
Bai F, Zhang Z, Yu H, Shi Y, Yuan Y, Zhu W, et al. Default-mode network activity distinguishes amnestic type mild cognitive impairment from healthy aging: a combined structural and resting-state functional MRI study. Neurosci Lett 438(1): 111-5. (2008).
[43]
Stavrou EP, Wood JM. Central visual field changes using flicker perimetry in type 2 diabetes mellitus. Acta Ophthalmol Scand 83(5): 574-80. (2005).
[44]
Olafsdottir E, Andersson DK, Stefansson E. Visual acuity in a population with regular screening for type 2 diabetes mellitus and eye disease. Acta Ophthalmol Scand 85(1): 40-5. (2007).
[45]
Hove MN, Kristensen JK, Lauritzen T, Bek T. Quantitative analysis of retinopathy in type 2 diabetes: identification of prognostic parameters for developing visual loss secondary to diabetic maculopathy. Acta Ophthalmol Scand 82(6): 679-85. (2004).
[46]
Liang Y, Chen Y, Li H, Zhao T, Sun X, Shu N, et al. Disrupted functional connectivity related to differential degeneration of the cingulum bundle in mild cognitive impairment patients. Curr Alzheimer Res 12(3): 255-65. (2015).
[47]
Lockhart SN, Mayda AB, Roach AE, Fletcher E, Carmichael O, Maillard P, et al. Episodic memory function is associated with multiple measures of white matter integrity in cognitive aging. Front Hum Neurosci 6: 56. (2012).
[48]
Medina D, DeToledo-Morrell L, Urresta F, Gabrieli JD, Moseley M, Fleischman D, et al. White matter changes in mild cognitive impairment and AD: A diffusion tensor imaging study. Neurobiol Aging 27(5): 663-72. (2006).
[49]
Remy F, Vayssiere N, Saint-Aubert L, Barbeau E, Pariente J. White matter disruption at the prodromal stage of Alzheimer’s disease: relationships with hippocampal atrophy and episodic memory performance. Neuroimage Clin 7: 482-92. (2015).
[50]
Hoogenboom WS, Marder TJ, Flores VL, Huisman S, Eaton HP, Schneiderman JS, et al. Cerebral white matter integrity and resting-state functional connectivity in middle-aged patients with type 2 diabetes. Diabetes 63(2): 728-38. (2014).
[51]
Chen Y, Liu Z, Zhang J, Tian G, Li L, Zhang S, et al. Selectively disrupted functional connectivity networks in type 2 diabetes mellitus. Front Aging Neurosci 7: 233. (2015).
[52]
Zhuang L, Sachdev PS, Trollor JN, Kochan NA, Reppermund S, Brodaty H, et al. Microstructural white matter changes in cognitively normal individuals at risk of amnestic MCI. Neurology 79(8): 748-54. (2012).