Hyperactivation of working memory-related brain circuits in newly diagnosed middle-aged type 2 diabetics

详细信息    查看全文

• 作者：Xiao-Song He (1) (5)
  Zhao-Xin Wang (1) (6)
  You-Zhi Zhu (2)
  Nan Wang (3)
  Xiaoping Hu (4)
  Da-Ren Zhang (1)
  De-Fa Zhu (3)
  Jiang-Ning Zhou (1)
  
  1. CAS Key Laboratory of Brain Function and Diseases ; School of Life Science ; University of Science and Technology of China ; 433 Huangshan Road ; Hefei ; 230027 ; Anhui ; China
  5. Key Laboratory of Behavioral Science ; Institute of Psychology ; Chinese Academy of Sciences ; Beijing ; China
  6. Key Laboratory of Brain Functional Genomics (MOE and STCSM) ; Institute of Cognitive Neuroscience ; School of Psychology and Cognitive Science ; East China Normal University ; Shanghai ; China
  2. Department of Radiology ; PLA 105 Hospital ; Hefei ; Anhui ; China
  3. Department of Endocrinology ; Anhui Geriatric Institute ; The First Affiliated Hospital of Anhui Medical University ; 218 Jixi Road ; Hefei ; 230022 ; Anhui ; China
  4. Department of Biomedical Engineering ; Georgia Tech and Emory University ; Atlanta ; GA ; USA
  
• 关键词：Type 2 diabetes ; Chronic hyperglycemia ; Working memory ; Functional magnetic resonance imaging (fMRI)
• 刊名：Acta Diabetologica
• 出版年：2015
• 出版时间：February 2015
• 年：2015
• 卷：52
• 期：1
• 页码：133-142
• 全文大小：666 KB
• 参考文献：1. McCrimmon RJ, Ryan CM, Frier BM (2012) Diabetes and cognitive dysfunction. Lancet 379:2291鈥?299 CrossRef
  2. Biessels GJ, Deary IJ, Ryan CM (2008) Cognition and diabetes: a lifespan perspective. Lancet Neurol 7:184鈥?90 CrossRef
  3. Heni M, Schopfer P, Peter A, Sartorius T, Fritsche A, Synofzik M, Haring HU, Maetzler W, Hennige AM (2013) Evidence for altered transport of insulin across the blood鈥揵rain barrier in insulin-resistant humans. Acta Diabetol. doi:10.1007/s00592-013-0546-y
  4. Biessels G (2007) Diabetic encephalopathy. In: Veves A, Malik R (eds) Diabetic neuropathy. Humana Press, New York, pp 187鈥?05 CrossRef
  5. Sima AA (2010) Encephalopathies: the emerging diabetic complications. Acta Diabetol 47:279鈥?93 CrossRef
  6. Ryan CM, Geckle MO (2000) Circumscribed cognitive dysfunction in middle-aged adults with type 2 diabetes. Diabetes Care 23:1486鈥?493 CrossRef
  7. Mogi N, Umegaki H, Hattori A, Maeda N, Miura H, Kuzuya M, Shimokata H, Ando F, Ito H, Iguchi A (2004) Cognitive function in Japanese elderly with type 2 diabetes mellitus. J Diabetes Complicat 18:42鈥?6 CrossRef
  8. Sommerfield AJ, Deary IJ, Frier BM (2004) Acute hyperglycemia alters mood state and impairs cognitive performance in people with type 2 diabetes. Diabetes Care 27:2335鈥?340 CrossRef
  9. Manschot SM, Brands AM, van der Grond J, Kessels RP, Algra A, Kappelle LJ, Biessels GJ, Utrecht Diabetic Encephalopathy Study G (2006) Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 55:1106鈥?113
  10. Moran C, Phan TG, Chen J, Blizzard L, Beare R, Venn A, Munch G, Wood AG, Forbes J, Greenaway TM, Pearson S, Srikanth V (2013) Brain atrophy in type 2 diabetes: regional distribution and influence on cognition. Diabetes Care 36:4036鈥?042 CrossRef
  11. van Elderen SG, de Roos A, de Craen AJ, Westendorp RG, Blauw GJ, Jukema JW, Bollen EL, Middelkoop HA, van Buchem MA, van der Grond J (2010) Progression of brain atrophy and cognitive decline in diabetes mellitus: a 3-year follow-up. Neurology 75:997鈥?002 CrossRef
  12. Dey J, Misra A, Desai NG, Mahapatra AK, Padma MV (1997) Cognitive function in younger type 2 diabetes. Diabetes Care 20:32鈥?5 CrossRef
  13. Cox DJ, Kovatchev BP, Gonder-Frederick LA, Summers KH, McCall A, Grimm KJ, Clarke WL (2005) Relationships between hyperglycemia and cognitive performance among adults with type 1 and type 2 diabetes. Diabetes Care 28:71鈥?7 CrossRef
  14. Arvanitakis Z, Wilson RS, Li Y, Aggarwal NT, Bennett DA (2006) Diabetes and function in different cognitive systems in older individuals without dementia. Diabetes Care 29:560鈥?65 CrossRef
  15. Bruehl H, Rueger M, Dziobek I, Sweat V, Tirsi A, Javier E, Arentoft A, Wolf OT, Convit A (2007) Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J Clin Endocrinol Metab 92:2439鈥?445 CrossRef
  16. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A (2009) Modifiers of cognitive function and brain structure in middle-aged and elderly individuals with type 2 diabetes mellitus. Brain Res 1280:186鈥?94 CrossRef
  17. Arvanitakis Z, Bennett DA, Wilson RS, Barnes LL (2010) Diabetes and cognitive systems in older black and white persons. Alzheimer Dis Assoc Disord 24:37鈥?2 CrossRef
  18. Chen Z, Li L, Sun J, Ma L (2012) Mapping the brain in type 2 diabetes: voxel-based morphometry using DARTEL. Eur J Radiol 81:1870鈥?876 CrossRef
  19. Hoogenboom WS, Marder TJ, Flores VL, Huisman S, Eaton HP, Schneiderman JS, Bolo NR, Simonson DC, Jacobson AM, Kubicki M, Shenton ME, Musen G (2014) Cerebral white matter integrity and resting-state functional connectivity in middle-aged patients with type 2 diabetes. Diabetes 63:728鈥?38 CrossRef
  20. Musen G, Jacobson AM, Bolo NR, Simonson DC, Shenton ME, McCartney RL, Flores VL, Hoogenboom WS (2012) Resting-state brain functional connectivity is altered in type 2 diabetes. Diabetes 61:2375鈥?379 CrossRef
  21. Xia W, Wang S, Sun Z, Bai F, Zhou Y, Yang Y, Wang P, Huang Y, Yuan Y (2013) Altered baseline brain activity in type 2 diabetes: a resting-state fMRI study. Psychoneuroendocrinology 38:2493鈥?501 CrossRef
  22. Naor M, Steingruber HJ, Westhoff K, Schottenfeld-Naor Y, Gries AF (1997) Cognitive function in elderly non-insulin-dependent diabetic patients before and after inpatient treatment for metabolic control. J Diabetes Complicat 11:40鈥?6 CrossRef
  23. Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25:46鈥?9 CrossRef
  24. Zhu DF, Wang ZX, Zhang DR, Pan ZL, He S, Hu XP, Chen XC, Zhou JN (2006) fMRI revealed neural substrate for reversible working memory dysfunction in subclinical hypothyroidism. Brain 129:2923鈥?930 CrossRef
  25. Lee JH, Yoon S, Renshaw PF, Kim TS, Jung JJ, Choi Y, Kim BN, Jacobson AM, Lyoo IK (2013) Morphometric changes in lateral ventricles of patients with recent-onset type 2 diabetes mellitus. PLoS ONE 8:e60515 CrossRef
  26. Last D, Alsop DC, Abduljalil AM, Marquis RP, de Bazelaire C, Hu K, Cavallerano J, Novak V (2007) Global and regional effects of type 2 diabetes on brain tissue volumes and cerebral vasoreactivity. Diabetes Care 30:1193鈥?199 CrossRef
  27. Smith EE, Jonides J, Marshuetz C, Koeppe RA (1998) Components of verbal working memory: evidence from neuroimaging. Proc Natl Acad Sci USA 95:876鈥?82 CrossRef
  28. D鈥橢sposito M, Postle BR, Rypma B (2000) Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp Brain Res 133:3鈥?1 CrossRef
  29. Cabeza R, Daselaar SM, Dolcos F, Prince SE, 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鈥?75 CrossRef
  30. Emery L, Heaven TJ, Paxton JL, Braver TS (2008) Age-related changes in neural activity during performance matched working memory manipulation. Neuroimage 42:1577鈥?586 CrossRef
  31. He XS, Ma N, Pan ZL, Wang ZX, Li N, Zhang XC, Zhou JN, Zhu DF, Zhang DR (2011) Functional magnetic resource imaging assessment of altered brain function in hypothyroidism during working memory processing. Eur J Endocrinol 164:951鈥?59 CrossRef
  32. Koenig RJ, Peterson CM, Jones RL, Saudek C, Lehrman M, Cerami A (1976) Correlation of glucose regulation and hemoglobin AIc in diabetes mellitus. N Engl J Med 295:417鈥?20 CrossRef
  33. Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15:539鈥?53 CrossRef
  34. Ashburner J, Friston KJ (2000) Voxel-based morphometry鈥攖he methods. Neuroimage 11:805鈥?21 CrossRef
  35. Levy JC, Matthews DR, Hermans MP (1998) Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21:2191鈥?192 CrossRef
  36. Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27:1487鈥?495 CrossRef
  37. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162鈥?73 CrossRef
  38. Wang ZX, Zhang JX, Wu QL, Liu N, Hu XP, Chan RC, Xiao ZW (2010) Alterations in the processing of non-drug-related affective stimuli in abstinent heroin addicts. Neuroimage 49:971鈥?76 CrossRef
  39. Wessels AM, Rombouts SA, Simsek S, Kuijer JP, Kostense PJ, Barkhof F, Scheltens P, Snoek FJ, Heine RJ (2006) Microvascular disease in type 1 diabetes alters brain activation: a functional magnetic resonance imaging study. Diabetes 55:334鈥?40 CrossRef
  40. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, Bertram L, Mullin K, Tanzi RE, Blacker D, Albert MS, Sperling RA (2005) Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65:404鈥?11 CrossRef
  41. Sperling R (2007) Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer鈥檚 disease. Ann N Y Acad Sci 1097:146鈥?55 CrossRef
  42. Dickerson BC, Salat DH, Bates JF, Atiya M, Killiany RJ, Greve DN, Dale AM, Stern CE, Blacker D, Albert MS, Sperling RA (2004) Medial temporal lobe function and structure in mild cognitive impairment. Ann Neurol 56:27鈥?5 CrossRef
  43. Hamalainen A, Pihlajamaki M, Tanila H, Hanninen T, Niskanen E, Tervo S, Karjalainen PA, Vanninen RL, Soininen H (2007) Increased fMRI responses during encoding in mild cognitive impairment. Neurobiol Aging 28:1889鈥?903 CrossRef
  44. Miller SL, Fenstermacher E, Bates J, Blacker D, Sperling RA, Dickerson BC (2008) Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J Neurol Neurosurg Psychiatry 79:630鈥?35 CrossRef
  45. O鈥橞rien JL, O鈥橩eefe KM, LaViolette PS, DeLuca AN, Blacker D, Dickerson BC, Sperling RA (2010) Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology 74:1969鈥?976 CrossRef
  46. Ryan JP, Fine DF, Rosano C (2014) Type 2 diabetes and cognitive impairment: contributions from neuroimaging. J Geriatr Psychiatry Neurol 27:47鈥?5 CrossRef
  47. Gruetter R, Ugurbil K, Seaquist ER (2000) Effect of acute hyperglycemia on visual cortical activation as measured by functional MRI. J Neurosci Res 62:279鈥?85 CrossRef
  48. Ebady SA, Arami MA, Shafigh MH (2008) Investigation on the relationship between diabetes mellitus type 2 and cognitive impairment. Diabetes Res Clin Pract 82:305鈥?09 CrossRef
  49. Cukierman-Yaffe T, Gerstein HC, Williamson JD, Lazar RM, Lovato L, Miller ME, Coker LH, Murray A, Sullivan MD, Marcovina SM, Launer LJ (2009) Relationship between baseline glycemic control and cognitive function in individuals with type 2 diabetes and other cardiovascular risk factors: the action to control cardiovascular risk in diabetes-memory in diabetes (ACCORD-MIND) trial. Diabetes Care 32:221鈥?26 CrossRef
  50. Ishizawa KT, Kumano H, Sato A, Sakura H, Iwamoto Y (2010) Decreased response inhibition in middle-aged male patients with type 2 diabetes. Biopsychosoc Med 4:1 CrossRef
  51. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167鈥?02 CrossRef
  52. Smith EE, Jonides J (1999) Storage and executive processes in the frontal lobes. Science 283:1657鈥?661 CrossRef
  53. Bruehl H, Sweat V, Tirsi A, Shah B, Convit A (2011) Obese adolescents with type 2 diabetes mellitus have hippocampal and frontal lobe volume reductions. Neurosci Med 2:34鈥?2 CrossRef
  54. Strachan MW, Reynolds RM, Frier BM, Mitchell RJ, Price JF (2008) The relationship between type 2 diabetes and dementia. Br Med Bull 88:131鈥?46 CrossRef
  55. Gjedde A, Crone C (1981) Blood鈥揵rain glucose transfer: repression in chronic hyperglycemia. Science 214:456鈥?57 CrossRef
  56. Duckrow RB, Beard DC, Brennan RW (1987) Regional cerebral blood flow decreases during chronic and acute hyperglycemia. Stroke 18:52鈥?8 CrossRef
  57. Jakobsen J, Nedergaard M, Aarslew-Jensen M, Diemer NH (1990) Regional brain glucose metabolism and blood flow in streptozocin-induced diabetic rats. Diabetes 39:437鈥?40 CrossRef
  58. Gispen WH, Biessels GJ (2000) Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23:542鈥?49 CrossRef
  59. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813鈥?20 CrossRef
  60. Zhao B, Pan BS, Shen SW, Sun X, Hou ZZ, Yan R, Sun FY (2013) Diabetes-induced central neuritic dystrophy and cognitive deficits are associated with the formation of oligomeric reticulon-3 via oxidative stress. J Biol Chem 288:15590鈥?5599 CrossRef
  61. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP (2008) Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 11:309鈥?17 CrossRef
  62. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P (2006) Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 5:64鈥?4 CrossRef
  63. Brundel M, Kappelle LJ, Biessels GJ (2014) Brain imaging in type 2 diabetes. Eur Neuropsychopharmacol. doi:10.1016/j.euroneuro.2014.01.023
  64. Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O鈥橞rien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M, nEuroimaging STfRVco (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822鈥?38 CrossRef
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Internal Medicine
  Diabetes
  Metabolic Diseases
  
• 出版者：Springer Milan
• ISSN：1432-5233

文摘

Type 2 diabetes mellitus (T2DM) is well known for its adverse impacts on brain and cognition, which leads to multidimensional cognitive deficits and wildly spread cerebral structure abnormalities. However, existing literatures are mainly focused on patients with advanced age or extended T2DM duration. Therefore, it remains unclear whether and how brain function would be affected at the initial onset stage of T2DM in relatively younger population. In current study, twelve newly diagnosed middle-aged T2DM patients with no previous diabetic treatment history and twelve matched controls were recruited. Brain activations during a working memory task, the digit n-back paradigm (0-, 1- and 2-back), were obtained with functional magnetic resonance imaging and tested by repeated measures ANOVA. Whereas patients performed the n-back task comparably well as controls, significant load-by-group interactions of brain activation were found in the right dorsolateral prefrontal cortex (DLPFC), left middle/inferior frontal gyrus, and left parietal cortex, where patients exhibited hyperactivation in the 2-back, but not the 0-back or 1-back condition compared to controls. Furthermore, the severity of chronic hyperglycemia, estimated by glycosylated hemoglobin (HbA1c) level, was entered into partial correlational analyses with task-related brain activations, while controlling for the real-time influence of glucose, estimated by instant plasma glucose level measured before scanning. Significant positive correlations were found between HbA1c and brain activations in the anterior cingulate cortex and bilateral DLPFC only in patients. Taken together, these findings suggest there might be a compensatory mechanism due to brain inefficiency related to chronic hyperglycemia at the initial onset stage of T2DM.