Skip to main content
Erschienen in: Current Diabetes Reports 9/2016

01.09.2016 | Microvascular Complications—Neuropathy (R Pop-Busui, Section Editor)

Diabetes and Cognitive Impairment

verfasst von: Lindsay A. Zilliox, Krish Chadrasekaran, Justin Y. Kwan, James W. Russell

Erschienen in: Current Diabetes Reports | Ausgabe 9/2016

Einloggen, um Zugang zu erhalten

Abstract

Both type 1 (T1DM) and type 2 diabetes mellitus (T2DM) have been associated with reduced performance on multiple domains of cognitive function and with evidence of abnormal structural and functional brain magnetic resonance imaging (MRI). Cognitive deficits may occur at the very earliest stages of diabetes and are further exacerbated by the metabolic syndrome. The duration of diabetes and glycemic control may have an impact on the type and severity of cognitive impairment, but as yet we cannot predict who is at greatest risk of developing cognitive impairment. The pathophysiology of cognitive impairment is multifactorial, although dysfunction in each interconnecting pathway ultimately leads to discordance in metabolic signaling. The pathophysiology includes defects in insulin signaling, autonomic function, neuroinflammatory pathways, mitochondrial (Mt) metabolism, the sirtuin-peroxisome proliferator-activated receptor-gamma co-activator 1α (SIRT-PGC-1α) axis, and Tau signaling. Several promising therapies have been identified in pre-clinical studies, but remain to be validated in clinical trials.
Literatur
1.
Zurück zum Zitat Wong RH, Scholey A, Howe PR. Assessing premorbid cognitive ability in adults with type 2 diabetes mellitus—a review with implications for future intervention studies. Curr Diab Rep. 2014;14(11):547–0547.PubMedCrossRef Wong RH, Scholey A, Howe PR. Assessing premorbid cognitive ability in adults with type 2 diabetes mellitus—a review with implications for future intervention studies. Curr Diab Rep. 2014;14(11):547–0547.PubMedCrossRef
2.
Zurück zum Zitat Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol. 2006;5(1):64–74.PubMedCrossRef Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol. 2006;5(1):64–74.PubMedCrossRef
3.
Zurück zum Zitat Grunblatt E, Bartl J, Riederer P. The link between iron, metabolic syndrome, and Alzheimer's disease. J Neural Transm. 2010;118(3):371-79. Grunblatt E, Bartl J, Riederer P. The link between iron, metabolic syndrome, and Alzheimer's disease. J Neural Transm. 2010;118(3):371-79.
4.••
Zurück zum Zitat Monette MC, Baird A, Jackson DL. A meta-analysis of cognitive functioning in nondemented adults with type 2 diabetes mellitus. Can J Diabetes. 2014;38(6):401–8. This study examines the pattern and magnitude of cognitive functioning deficits in persons withT2DM without dementia using meta-analysis.PubMedCrossRef Monette MC, Baird A, Jackson DL. A meta-analysis of cognitive functioning in nondemented adults with type 2 diabetes mellitus. Can J Diabetes. 2014;38(6):401–8. This study examines the pattern and magnitude of cognitive functioning deficits in persons withT2DM without dementia using meta-analysis.PubMedCrossRef
5.
Zurück zum Zitat Palta P, Schneider AL, Biessels GJ, Touradji P, Hill-Briggs F. Magnitude of cognitive dysfunction in adults with type 2 diabetes: a meta-analysis of six cognitive domains and the most frequently reported neuropsychological tests within domains. J Int Neuropsychol Soc. 2014;20(3):278–91.PubMedPubMedCentralCrossRef Palta P, Schneider AL, Biessels GJ, Touradji P, Hill-Briggs F. Magnitude of cognitive dysfunction in adults with type 2 diabetes: a meta-analysis of six cognitive domains and the most frequently reported neuropsychological tests within domains. J Int Neuropsychol Soc. 2014;20(3):278–91.PubMedPubMedCentralCrossRef
6.
Zurück zum Zitat Dik MG, Jonker C, Comijs HC, Deeg DJ, Kok A, Yaffe K, et al. Contribution of metabolic syndrome components to cognition in older individuals. Diabetes Care. 2007;30(10):2655–60.PubMedCrossRef Dik MG, Jonker C, Comijs HC, Deeg DJ, Kok A, Yaffe K, et al. Contribution of metabolic syndrome components to cognition in older individuals. Diabetes Care. 2007;30(10):2655–60.PubMedCrossRef
7.
Zurück zum Zitat Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP. The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement. 2013;9(1):63–75.PubMedCrossRef Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP. The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement. 2013;9(1):63–75.PubMedCrossRef
9.
Zurück zum Zitat Rawlings AM, Sharrett AR, Schneider AL, Coresh J, Albert M, Couper D, et al. Diabetes in midlife and cognitive change over 20 years: a cohort study. Ann Intern Med. 2014;161(11):785–93.PubMedPubMedCentralCrossRef Rawlings AM, Sharrett AR, Schneider AL, Coresh J, Albert M, Couper D, et al. Diabetes in midlife and cognitive change over 20 years: a cohort study. Ann Intern Med. 2014;161(11):785–93.PubMedPubMedCentralCrossRef
11.
Zurück zum Zitat Chatterjee S, Peters SA, Woodward M, Mejia AS, Batty GD, Beckett N, et al. Type 2 diabetes as a risk factor for dementia in women compared with men: a pooled analysis of 2.3 million people comprising more than 100,000 cases of dementia. Diabetes Care. 2016;39(2):300–7.PubMed Chatterjee S, Peters SA, Woodward M, Mejia AS, Batty GD, Beckett N, et al. Type 2 diabetes as a risk factor for dementia in women compared with men: a pooled analysis of 2.3 million people comprising more than 100,000 cases of dementia. Diabetes Care. 2016;39(2):300–7.PubMed
12.
13.
Zurück zum Zitat Akter K, Lanza EA, Martin SA, Myronyuk N, Rua M, Raffa RB. Diabetes mellitus and Alzheimer’s disease: shared pathology and treatment? Br J Clin Pharmacol. 2011;71(3):365–76.PubMedPubMedCentralCrossRef Akter K, Lanza EA, Martin SA, Myronyuk N, Rua M, Raffa RB. Diabetes mellitus and Alzheimer’s disease: shared pathology and treatment? Br J Clin Pharmacol. 2011;71(3):365–76.PubMedPubMedCentralCrossRef
14.
Zurück zum Zitat Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology. 1999;53(9):1937–42.PubMedCrossRef Ott A, Stolk RP, van Harskamp F, Pols HA, Hofman A, Breteler MM. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology. 1999;53(9):1937–42.PubMedCrossRef
15.
Zurück zum Zitat Luchsinger JA. Adiposity, hyperinsulinemia, diabetes and Alzheimer’s disease: an epidemiological perspective. Eur J Pharmacol. 2008;585(1):119–29.PubMedPubMedCentralCrossRef Luchsinger JA. Adiposity, hyperinsulinemia, diabetes and Alzheimer’s disease: an epidemiological perspective. Eur J Pharmacol. 2008;585(1):119–29.PubMedPubMedCentralCrossRef
16.
17.
18.
Zurück zum Zitat Ohara T, Doi Y, Ninomiya T, Hirakawa Y, Hata J, Iwaki T, et al. Glucose tolerance status and risk of dementia in the community: the Hisayama study. Neurology. 2011;77(12):1126–34.PubMedCrossRef Ohara T, Doi Y, Ninomiya T, Hirakawa Y, Hata J, Iwaki T, et al. Glucose tolerance status and risk of dementia in the community: the Hisayama study. Neurology. 2011;77(12):1126–34.PubMedCrossRef
19.
Zurück zum Zitat Whitmer RA. Type 2 diabetes and risk of cognitive impairment and dementia. Curr Neurol Neurosci Rep. 2007;7(5):373–80.PubMedCrossRef Whitmer RA. Type 2 diabetes and risk of cognitive impairment and dementia. Curr Neurol Neurosci Rep. 2007;7(5):373–80.PubMedCrossRef
20.
Zurück zum Zitat Whitmer RA. The epidemiology of adiposity and dementia. Curr Alzheimer Res. 2007;4(2):117–22.PubMedCrossRef Whitmer RA. The epidemiology of adiposity and dementia. Curr Alzheimer Res. 2007;4(2):117–22.PubMedCrossRef
21.
Zurück zum Zitat Gustafson D, Rothenberg E, Blennow K, Steen B, Skoog I. An 18-year follow-up of overweight and risk of Alzheimer disease. Arch Intern Med. 2003;163(13):1524–8.PubMedCrossRef Gustafson D, Rothenberg E, Blennow K, Steen B, Skoog I. An 18-year follow-up of overweight and risk of Alzheimer disease. Arch Intern Med. 2003;163(13):1524–8.PubMedCrossRef
22.
Zurück zum Zitat Schnaider BM, Goldbourt U, Silverman JM, Noy S, Schmeidler J, Ravona-Springer R, et al. Diabetes mellitus in midlife and the risk of dementia three decades later. Neurology. 2004;63(10):1902–7.CrossRef Schnaider BM, Goldbourt U, Silverman JM, Noy S, Schmeidler J, Ravona-Springer R, et al. Diabetes mellitus in midlife and the risk of dementia three decades later. Neurology. 2004;63(10):1902–7.CrossRef
23.
Zurück zum Zitat Xu W, Caracciolo B, Wang HX, Winblad B, Backman L, Qiu C, et al. Accelerated progression from mild cognitive impairment to dementia in people with diabetes. Diabetes. 2010;59(11):2928–35.PubMedPubMedCentralCrossRef Xu W, Caracciolo B, Wang HX, Winblad B, Backman L, Qiu C, et al. Accelerated progression from mild cognitive impairment to dementia in people with diabetes. Diabetes. 2010;59(11):2928–35.PubMedPubMedCentralCrossRef
24.
Zurück zum Zitat Kanaya AM, Barrett-Connor E, Gildengorin G, Yaffe K. Change in cognitive function by glucose tolerance status in older adults: a 4-year prospective study of the Rancho Bernardo study cohort. Arch Intern Med. 2004;164(12):1327–33.PubMedCrossRef Kanaya AM, Barrett-Connor E, Gildengorin G, Yaffe K. Change in cognitive function by glucose tolerance status in older adults: a 4-year prospective study of the Rancho Bernardo study cohort. Arch Intern Med. 2004;164(12):1327–33.PubMedCrossRef
25.
Zurück zum Zitat Gregg EW, Yaffe K, Cauley JA, Rolka DB, Blackwell TL, Narayan KM, et al. Is diabetes associated with cognitive impairment and cognitive decline among older women? Study of Osteoporotic Fractures Research Group. Arch Intern Med. 2000;160(2):174–80.PubMedCrossRef Gregg EW, Yaffe K, Cauley JA, Rolka DB, Blackwell TL, Narayan KM, et al. Is diabetes associated with cognitive impairment and cognitive decline among older women? Study of Osteoporotic Fractures Research Group. Arch Intern Med. 2000;160(2):174–80.PubMedCrossRef
26.
Zurück zum Zitat van den Berg E, Reijmer YD, de Bresser J, Kessels RP, Kappelle LJ, Biessels GJ. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia. 2010;53(1):58–65.PubMedCrossRef van den Berg E, Reijmer YD, de Bresser J, Kessels RP, Kappelle LJ, Biessels GJ. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia. 2010;53(1):58–65.PubMedCrossRef
27.
Zurück zum Zitat Garcia-Casares N, Jorge RE, Garcia-Arnes JA, Acion L, Berthier ML, Gonzalez-Alegre P, et al. Cognitive dysfunctions in middle-aged type 2 diabetic patients and neuroimaging correlations: a cross-sectional study. J Alzheimers Dis. 2014;42(4):1337–46.PubMed Garcia-Casares N, Jorge RE, Garcia-Arnes JA, Acion L, Berthier ML, Gonzalez-Alegre P, et al. Cognitive dysfunctions in middle-aged type 2 diabetic patients and neuroimaging correlations: a cross-sectional study. J Alzheimers Dis. 2014;42(4):1337–46.PubMed
29.
Zurück zum Zitat Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP. The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care. 2005;28(3):726–35.PubMedCrossRef Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP. The effects of type 1 diabetes on cognitive performance: a meta-analysis. Diabetes Care. 2005;28(3):726–35.PubMedCrossRef
30.
Zurück zum Zitat Yaffe K, Blackwell T, Kanaya AM, Davidowitz N, Barrett-Connor E, Krueger K. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology. 2004;63(4):658–63.PubMedCrossRef Yaffe K, Blackwell T, Kanaya AM, Davidowitz N, Barrett-Connor E, Krueger K. Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology. 2004;63(4):658–63.PubMedCrossRef
31.
Zurück zum Zitat Hassing LB, Grant MD, Hofer SM, Pedersen NL, Nilsson SE, Berg S, et al. Type 2 diabetes mellitus contributes to cognitive decline in old age: a longitudinal population-based study. J Int Neuropsychol Soc. 2004;10(4):599–607.PubMedCrossRef Hassing LB, Grant MD, Hofer SM, Pedersen NL, Nilsson SE, Berg S, et al. Type 2 diabetes mellitus contributes to cognitive decline in old age: a longitudinal population-based study. J Int Neuropsychol Soc. 2004;10(4):599–607.PubMedCrossRef
32.
Zurück zum Zitat Cukierman-Yaffe T, Gerstein HC, Williamson JD, Lazar RM, Lovato L, Miller ME, et al. 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. 2009;32(2):221–6.PubMedPubMedCentralCrossRef Cukierman-Yaffe T, Gerstein HC, Williamson JD, Lazar RM, Lovato L, Miller ME, et al. 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. 2009;32(2):221–6.PubMedPubMedCentralCrossRef
33.
Zurück zum Zitat Launer LJ, Miller ME, Williamson JD, Lazar RM, Gerstein HC, Murray AM, et al. Effects of intensive glucose lowering on brain structure and function in people with type 2 diabetes (ACCORD MIND): a randomised open-label substudy. Lancet Neurol. 2011;10(11):969–77.PubMedPubMedCentralCrossRef Launer LJ, Miller ME, Williamson JD, Lazar RM, Gerstein HC, Murray AM, et al. Effects of intensive glucose lowering on brain structure and function in people with type 2 diabetes (ACCORD MIND): a randomised open-label substudy. Lancet Neurol. 2011;10(11):969–77.PubMedPubMedCentralCrossRef
34.
Zurück zum Zitat Erus G, Battapady H, Zhang T, Lovato J, Miller ME, Williamson JD, et al. Spatial patterns of structural brain changes in type 2 diabetic patients and their longitudinal progression with intensive control of blood glucose. Diabetes Care. 2015;38(1):97–104.PubMedCrossRef Erus G, Battapady H, Zhang T, Lovato J, Miller ME, Williamson JD, et al. Spatial patterns of structural brain changes in type 2 diabetic patients and their longitudinal progression with intensive control of blood glucose. Diabetes Care. 2015;38(1):97–104.PubMedCrossRef
35.
Zurück zum Zitat Jacobson AM, Musen G, Ryan CM, Silvers N, Cleary P, Waberski B, et al. Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med. 2007;356(18):1842–52.PubMedCrossRef Jacobson AM, Musen G, Ryan CM, Silvers N, Cleary P, Waberski B, et al. Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med. 2007;356(18):1842–52.PubMedCrossRef
36.
Zurück zum Zitat Gaudieri PA, Chen R, Greer TF, Holmes CS. Cognitive function in children with type 1 diabetes: a meta-analysis. Diabetes Care. 2008;31(9):1892–7.PubMedPubMedCentralCrossRef Gaudieri PA, Chen R, Greer TF, Holmes CS. Cognitive function in children with type 1 diabetes: a meta-analysis. Diabetes Care. 2008;31(9):1892–7.PubMedPubMedCentralCrossRef
37.•
Zurück zum Zitat Choi J, Chandrasekaran K, Demarest TG, Kristian T, Xu S, Vijaykumar K, et al. Brain diabetic neurodegeneration segregates with low intrinsic aerobic capacity. Ann Clin Transl Neurol. 2014;1(8):589–604. This paper links mitochondrial p-tau hyperphosphorylation, a marker of AD, with mitochondrial dysfunction in the hippocampus in a rat model of T2DM.PubMedPubMedCentralCrossRef Choi J, Chandrasekaran K, Demarest TG, Kristian T, Xu S, Vijaykumar K, et al. Brain diabetic neurodegeneration segregates with low intrinsic aerobic capacity. Ann Clin Transl Neurol. 2014;1(8):589–604. This paper links mitochondrial p-tau hyperphosphorylation, a marker of AD, with mitochondrial dysfunction in the hippocampus in a rat model of T2DM.PubMedPubMedCentralCrossRef
38.
Zurück zum Zitat 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. 2014;37(12):3157–63.PubMedCrossRef 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. 2014;37(12):3157–63.PubMedCrossRef
39.
Zurück zum Zitat Cherbuin N, Sachdev P, Anstey KJ. Higher normal fasting plasma glucose is associated with hippocampal atrophy: The PATH Study. Neurology. 2012;79(10):1019–26.PubMedCrossRef Cherbuin N, Sachdev P, Anstey KJ. Higher normal fasting plasma glucose is associated with hippocampal atrophy: The PATH Study. Neurology. 2012;79(10):1019–26.PubMedCrossRef
40.
Zurück zum Zitat Biessels GJ, Reijmer YD. Brain changes underlying cognitive dysfunction in diabetes: what can we learn from MRI? Diabetes. 2014;63(7):2244–52.PubMedCrossRef Biessels GJ, Reijmer YD. Brain changes underlying cognitive dysfunction in diabetes: what can we learn from MRI? Diabetes. 2014;63(7):2244–52.PubMedCrossRef
41.
Zurück zum Zitat Marjanska M, Curran GL, Wengenack TM, Henry PG, Bliss RL, Poduslo JF, et al. Monitoring disease progression in transgenic mouse models of Alzheimer’s disease with proton magnetic resonance spectroscopy. Proc Natl Acad Sci U S A. 2005;102(33):11906–10.PubMedPubMedCentralCrossRef Marjanska M, Curran GL, Wengenack TM, Henry PG, Bliss RL, Poduslo JF, et al. Monitoring disease progression in transgenic mouse models of Alzheimer’s disease with proton magnetic resonance spectroscopy. Proc Natl Acad Sci U S A. 2005;102(33):11906–10.PubMedPubMedCentralCrossRef
42.
Zurück zum Zitat Xu S, Zhuo J, Racz J, Shi D, Roys S, Fiskum G, et al. Early microstructural and metabolic changes following controlled cortical impact injury in rat: a magnetic resonance imaging and spectroscopy study. J Neurotrauma. 2011;28(10):2091–102.PubMedPubMedCentralCrossRef Xu S, Zhuo J, Racz J, Shi D, Roys S, Fiskum G, et al. Early microstructural and metabolic changes following controlled cortical impact injury in rat: a magnetic resonance imaging and spectroscopy study. J Neurotrauma. 2011;28(10):2091–102.PubMedPubMedCentralCrossRef
43.
Zurück zum Zitat Santhakumari R, Reddy IY, Archana R. Effect of type 2 diabetes mellitus on brain metabolites by using proton magnetic resonance spectroscopy a systematic review. Int J Pharma Bio Sci. 2014;5(4):1118–23.PubMedPubMedCentral Santhakumari R, Reddy IY, Archana R. Effect of type 2 diabetes mellitus on brain metabolites by using proton magnetic resonance spectroscopy a systematic review. Int J Pharma Bio Sci. 2014;5(4):1118–23.PubMedPubMedCentral
44.
Zurück zum Zitat Abbott MA, Wells DG, Fallon JR. The insulin receptor tyrosine kinase substrate p58/53 and the insulin receptor are components of CNS synapses. J Neurosci. 1999;19(17):7300–8.PubMed Abbott MA, Wells DG, Fallon JR. The insulin receptor tyrosine kinase substrate p58/53 and the insulin receptor are components of CNS synapses. J Neurosci. 1999;19(17):7300–8.PubMed
45.
Zurück zum Zitat Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Mendelsohn FA. Localization and characterization of Insulin-Like Growth Factor-I Receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry* a distinct distribution from insulin receptors. J Neuroendocrinol. 1989;1(5):369–77.PubMedCrossRef Werther GA, Hogg A, Oldfield BJ, McKinley MJ, Figdor R, Mendelsohn FA. Localization and characterization of Insulin-Like Growth Factor-I Receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry* a distinct distribution from insulin receptors. J Neuroendocrinol. 1989;1(5):369–77.PubMedCrossRef
46.
Zurück zum Zitat Zhao W, Chen H, Xu H, Moore E, Meiri N, Quon MJ, et al. Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J Biol Chem. 1999;274(49):34893–902.PubMedCrossRef Zhao W, Chen H, Xu H, Moore E, Meiri N, Quon MJ, et al. Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J Biol Chem. 1999;274(49):34893–902.PubMedCrossRef
47.
Zurück zum Zitat Baskin DG, Figlewicz DP, Woods SC, Porte Jr D, Dorsa DM. Insulin in the brain. Annu Rev Physiol. 1987;49:335–47.PubMedCrossRef Baskin DG, Figlewicz DP, Woods SC, Porte Jr D, Dorsa DM. Insulin in the brain. Annu Rev Physiol. 1987;49:335–47.PubMedCrossRef
49.
Zurück zum Zitat Woods SC, Seeley RJ, Baskin DG, Schwartz MW. Insulin and the blood-brain barrier. Curr Pharm Des. 2003;9(10):795–800.PubMedCrossRef Woods SC, Seeley RJ, Baskin DG, Schwartz MW. Insulin and the blood-brain barrier. Curr Pharm Des. 2003;9(10):795–800.PubMedCrossRef
50.
Zurück zum Zitat Devaskar SU, Giddings SJ, Rajakumar PA, Carnaghi LR, Menon RK, Zahm DS. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J Biol Chem. 1994;269(11):8445–54.PubMed Devaskar SU, Giddings SJ, Rajakumar PA, Carnaghi LR, Menon RK, Zahm DS. Insulin gene expression and insulin synthesis in mammalian neuronal cells. J Biol Chem. 1994;269(11):8445–54.PubMed
51.
Zurück zum Zitat Devaskar SU, Singh BS, Carnaghi LR, Rajakumar PA, Giddings SJ. Insulin II gene expression in rat central nervous system. Regul Pept. 1993;48:55–63.PubMedCrossRef Devaskar SU, Singh BS, Carnaghi LR, Rajakumar PA, Giddings SJ. Insulin II gene expression in rat central nervous system. Regul Pept. 1993;48:55–63.PubMedCrossRef
52.
Zurück zum Zitat Kuwabara T, Kagalwala MN, Onuma Y, Ito Y, Warashina M, Terashima K, et al. Insulin biosynthesis in neuronal progenitors derived from adult hippocampus and the olfactory bulb. EMBO Mol Med. 2011;3(12):742–54.PubMedPubMedCentralCrossRef Kuwabara T, Kagalwala MN, Onuma Y, Ito Y, Warashina M, Terashima K, et al. Insulin biosynthesis in neuronal progenitors derived from adult hippocampus and the olfactory bulb. EMBO Mol Med. 2011;3(12):742–54.PubMedPubMedCentralCrossRef
53.
Zurück zum Zitat Skeberdis VA, Lan J, Zheng X, Zukin RS, Bennett MV. Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis. Proc Natl Acad Sci U S A. 2001;98(6):3561–6.PubMedPubMedCentralCrossRef Skeberdis VA, Lan J, Zheng X, Zukin RS, Bennett MV. Insulin promotes rapid delivery of N-methyl-D- aspartate receptors to the cell surface by exocytosis. Proc Natl Acad Sci U S A. 2001;98(6):3561–6.PubMedPubMedCentralCrossRef
54.
Zurück zum Zitat Boyd Jr FT, Clarke DW, Muther TF, Raizada MK. Insulin receptors and insulin modulation of norepinephrine uptake in neuronal cultures from rat brain. J Biol Chem. 1985;260(29):15880–4.PubMed Boyd Jr FT, Clarke DW, Muther TF, Raizada MK. Insulin receptors and insulin modulation of norepinephrine uptake in neuronal cultures from rat brain. J Biol Chem. 1985;260(29):15880–4.PubMed
55.
Zurück zum Zitat Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, et al. Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature. 1997;388(6643):686–90.PubMedCrossRef Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, et al. Recruitment of functional GABA(A) receptors to postsynaptic domains by insulin. Nature. 1997;388(6643):686–90.PubMedCrossRef
56.
Zurück zum Zitat Marks DR, Tucker K, Cavallin MA, Mast TG, Fadool DA. Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J Neurosci. 2009;29(20):6734–51.PubMedPubMedCentralCrossRef Marks DR, Tucker K, Cavallin MA, Mast TG, Fadool DA. Awake intranasal insulin delivery modifies protein complexes and alters memory, anxiety, and olfactory behaviors. J Neurosci. 2009;29(20):6734–51.PubMedPubMedCentralCrossRef
57.
Zurück zum Zitat Shemesh E, Rudich A, Harman-Boehm I, Cukierman-Yaffe T. Effect of intranasal insulin on cognitive function: a systematic review. J Clin Endocrinol Metab. 2012;97(2):366–76.PubMedCrossRef Shemesh E, Rudich A, Harman-Boehm I, Cukierman-Yaffe T. Effect of intranasal insulin on cognitive function: a systematic review. J Clin Endocrinol Metab. 2012;97(2):366–76.PubMedCrossRef
59.
Zurück zum Zitat Calvo-Ochoa E, Arias C. Cellular and metabolic alterations in the hippocampus caused by insulin signalling dysfunction and its association with cognitive impairment during aging and Alzheimer’s disease: studies in animal models. Diabetes Metab Res Rev. 2015;31(1):1–13.PubMedCrossRef Calvo-Ochoa E, Arias C. Cellular and metabolic alterations in the hippocampus caused by insulin signalling dysfunction and its association with cognitive impairment during aging and Alzheimer’s disease: studies in animal models. Diabetes Metab Res Rev. 2015;31(1):1–13.PubMedCrossRef
60.
Zurück zum Zitat Heras-Sandoval D, Ferrera P, Arias C. Amyloid-beta protein modulates insulin signaling in presynaptic terminals. Neurochem Res. 2012;37(9):1879–85.PubMedCrossRef Heras-Sandoval D, Ferrera P, Arias C. Amyloid-beta protein modulates insulin signaling in presynaptic terminals. Neurochem Res. 2012;37(9):1879–85.PubMedCrossRef
61.
Zurück zum Zitat Choi J, Malakowsky CA, Talent JM, Conrad CC, Gracy RW. Identification of oxidized plasma proteins in Alzheimer’s disease. Biochem Biophys Res Commun. 2002;293(5):1566–70.PubMedCrossRef Choi J, Malakowsky CA, Talent JM, Conrad CC, Gracy RW. Identification of oxidized plasma proteins in Alzheimer’s disease. Biochem Biophys Res Commun. 2002;293(5):1566–70.PubMedCrossRef
62.
Zurück zum Zitat Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, et al. Gene regulation and DNA damage in the ageing human brain. Nature. 2004;429(6994):883–91.PubMedCrossRef Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, et al. Gene regulation and DNA damage in the ageing human brain. Nature. 2004;429(6994):883–91.PubMedCrossRef
63.
Zurück zum Zitat Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J Neurosci. 2009;29(28):9090–103.PubMedPubMedCentralCrossRef Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J Neurosci. 2009;29(28):9090–103.PubMedPubMedCentralCrossRef
64.
Zurück zum Zitat Su B, Wang X, Zheng L, Perry G, Smith MA, Zhu X. Abnormal mitochondrial dynamics and neurodegenerative diseases. Biochim Biophys Acta. 2010;1802(1):135–42.PubMedCrossRef Su B, Wang X, Zheng L, Perry G, Smith MA, Zhu X. Abnormal mitochondrial dynamics and neurodegenerative diseases. Biochim Biophys Acta. 2010;1802(1):135–42.PubMedCrossRef
65.
Zurück zum Zitat Chandrasekaran K, Hatanpaa K, Rapoport SI, Brady DR. Decreased expression of nuclear and mitochondrial DNA-encoded genes of oxidative phosphorylation in association neocortex in Alzheimer disease. Brain Res Mol Brain Res. 1997;44(1):99–104.PubMedCrossRef Chandrasekaran K, Hatanpaa K, Rapoport SI, Brady DR. Decreased expression of nuclear and mitochondrial DNA-encoded genes of oxidative phosphorylation in association neocortex in Alzheimer disease. Brain Res Mol Brain Res. 1997;44(1):99–104.PubMedCrossRef
66.
Zurück zum Zitat Kim B, Backus C, Oh S, Hayes JM, Feldman EL. Increased tau phosphorylation and cleavage in mouse models of type 1 and type 2 diabetes. Endocrinology. 2009;150(12):5294–301.PubMedPubMedCentralCrossRef Kim B, Backus C, Oh S, Hayes JM, Feldman EL. Increased tau phosphorylation and cleavage in mouse models of type 1 and type 2 diabetes. Endocrinology. 2009;150(12):5294–301.PubMedPubMedCentralCrossRef
67.
Zurück zum Zitat Eckert A, Schulz KL, Rhein V, Gotz J. Convergence of amyloid-beta and tau pathologies on mitochondria in vivo. Mol Neurobiol. 2010;41(2–3):107–14.PubMedPubMedCentralCrossRef Eckert A, Schulz KL, Rhein V, Gotz J. Convergence of amyloid-beta and tau pathologies on mitochondria in vivo. Mol Neurobiol. 2010;41(2–3):107–14.PubMedPubMedCentralCrossRef
68.
Zurück zum Zitat Choi J, Batchu VV, Schubert M, Castellani RJ, Russell JW. A novel PGC-1alpha isoform in brain localizes to mitochondria and associates with PINK1 and VDAC. Biochem Biophys Res Commun. 2013;435(4):671–7.PubMedPubMedCentralCrossRef Choi J, Batchu VV, Schubert M, Castellani RJ, Russell JW. A novel PGC-1alpha isoform in brain localizes to mitochondria and associates with PINK1 and VDAC. Biochem Biophys Res Commun. 2013;435(4):671–7.PubMedPubMedCentralCrossRef
70.
Zurück zum Zitat Wilhelmus MM, van der Pol SM, Jansen Q, Witte ME, van der Valk P, Rozemuller AJ et al. Association of Parkinson disease-related protein PINK1 with Alzheimer disease and multiple sclerosis brain lesions. Free Radic Biol Med. 2011;50(3):469–76. Wilhelmus MM, van der Pol SM, Jansen Q, Witte ME, van der Valk P, Rozemuller AJ et al. Association of Parkinson disease-related protein PINK1 with Alzheimer disease and multiple sclerosis brain lesions. Free Radic Biol Med. 2011;50(3):469–76.
71.
Zurück zum Zitat Choi J, Chandrasekaran K, Inoue T, Muragundla A, Russell JW. PGC-1alpha regulation of mitochondrial degeneration in experimental diabetic neuropathy. Neurobiol Dis. 2014;64:118–30.PubMedPubMedCentralCrossRef Choi J, Chandrasekaran K, Inoue T, Muragundla A, Russell JW. PGC-1alpha regulation of mitochondrial degeneration in experimental diabetic neuropathy. Neurobiol Dis. 2014;64:118–30.PubMedPubMedCentralCrossRef
72.
Zurück zum Zitat Lin J, Wu PH, Tarr PT, Lindenberg KS, St Pierre J, Zhang CY, et al. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice.[see comment]. Cell. 2004;119(1):125–35.CrossRef Lin J, Wu PH, Tarr PT, Lindenberg KS, St Pierre J, Zhang CY, et al. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice.[see comment]. Cell. 2004;119(1):125–35.CrossRef
74.
Zurück zum Zitat Zaslavsky LM, Gross JL, Chaves ML, Machado R. Memory dysfunction and autonomic neuropathy in non-insulin-dependent (type 2) diabetic patients. Diabetes Res Clin Pract. 1995;30(2):101–10.PubMedCrossRef Zaslavsky LM, Gross JL, Chaves ML, Machado R. Memory dysfunction and autonomic neuropathy in non-insulin-dependent (type 2) diabetic patients. Diabetes Res Clin Pract. 1995;30(2):101–10.PubMedCrossRef
75.•
Zurück zum Zitat Nicolini P, Ciulla MM, Malfatto G, Abbate C, Mari D, Rossi PD, et al. Autonomic dysfunction in mild cognitive impairment: evidence from power spectral analysis of heart rate variability in a cross-sectional case-control study. PLoS One. 2014;9(5):e96656. The study links autonomic dysfunction with presence of MCI.PubMedPubMedCentralCrossRef Nicolini P, Ciulla MM, Malfatto G, Abbate C, Mari D, Rossi PD, et al. Autonomic dysfunction in mild cognitive impairment: evidence from power spectral analysis of heart rate variability in a cross-sectional case-control study. PLoS One. 2014;9(5):e96656. The study links autonomic dysfunction with presence of MCI.PubMedPubMedCentralCrossRef
77.
Zurück zum Zitat Frewen J, Finucane C, Savva GM, Boyle G, Coen RF, Kenny RA. Cognitive function is associated with impaired heart rate variability in ageing adults: the Irish longitudinal study on ageing wave one results. Clin Auton Res. 2013;23(6):313–23.PubMedCrossRef Frewen J, Finucane C, Savva GM, Boyle G, Coen RF, Kenny RA. Cognitive function is associated with impaired heart rate variability in ageing adults: the Irish longitudinal study on ageing wave one results. Clin Auton Res. 2013;23(6):313–23.PubMedCrossRef
78.
Zurück zum Zitat Guaraldi P, Poda R, Calandra-Buonaura G, Solieri L, Sambati L, Gallassi R, et al. Cognitive function in peripheral autonomic disorders. PLoS One. 2014;9(1):e85020.PubMedPubMedCentralCrossRef Guaraldi P, Poda R, Calandra-Buonaura G, Solieri L, Sambati L, Gallassi R, et al. Cognitive function in peripheral autonomic disorders. PLoS One. 2014;9(1):e85020.PubMedPubMedCentralCrossRef
79.
Zurück zum Zitat Gibbons CH, Centi J, Vernino S, Freeman R. Autoimmune autonomic ganglionopathy with reversible cognitive impairment. Arch Neurol. 2012;69(4):461–6.PubMedCrossRef Gibbons CH, Centi J, Vernino S, Freeman R. Autoimmune autonomic ganglionopathy with reversible cognitive impairment. Arch Neurol. 2012;69(4):461–6.PubMedCrossRef
80.••
Zurück zum Zitat Gaspar JM, Baptista FI, Macedo MP, Ambrosio AF. Inside the diabetic brain: role of different players involved in cognitive decline. ACS Chem Neurosci. 2016;7(2):131–42. This manuscript provides an in depth review of the current known pathways that can lead to impairment in cognition in the diabetic brain.PubMedCrossRef Gaspar JM, Baptista FI, Macedo MP, Ambrosio AF. Inside the diabetic brain: role of different players involved in cognitive decline. ACS Chem Neurosci. 2016;7(2):131–42. This manuscript provides an in depth review of the current known pathways that can lead to impairment in cognition in the diabetic brain.PubMedCrossRef
81.
Zurück zum Zitat Datusalia AK, Sharma SS. NF-kappaB inhibition resolves cognitive deficits in experimental type 2 diabetes mellitus through CREB and Glutamate/GABA neurotransmitters pathway. Curr Neurovasc Res. 2016;13(1):22–32.PubMedCrossRef Datusalia AK, Sharma SS. NF-kappaB inhibition resolves cognitive deficits in experimental type 2 diabetes mellitus through CREB and Glutamate/GABA neurotransmitters pathway. Curr Neurovasc Res. 2016;13(1):22–32.PubMedCrossRef
82.
Zurück zum Zitat Valente T, Gella A, Fernandez-Busquets X, Unzeta M, Durany N. Immunohistochemical analysis of human brain suggests pathological synergism of Alzheimer’s disease and diabetes mellitus. Neurobiol Dis. 2010;37(1):67–76.PubMedCrossRef Valente T, Gella A, Fernandez-Busquets X, Unzeta M, Durany N. Immunohistochemical analysis of human brain suggests pathological synergism of Alzheimer’s disease and diabetes mellitus. Neurobiol Dis. 2010;37(1):67–76.PubMedCrossRef
83.
Zurück zum Zitat Puig KL, Floden AM, Adhikari R, Golovko MY, Combs CK. Amyloid precursor protein and proinflammatory changes are regulated in brain and adipose tissue in a murine model of high fat diet-induced obesity. PLoS One. 2012;7(1):e30378.PubMedPubMedCentralCrossRef Puig KL, Floden AM, Adhikari R, Golovko MY, Combs CK. Amyloid precursor protein and proinflammatory changes are regulated in brain and adipose tissue in a murine model of high fat diet-induced obesity. PLoS One. 2012;7(1):e30378.PubMedPubMedCentralCrossRef
84.
Zurück zum Zitat Dinel AL, Andre C, Aubert A, Ferreira G, Laye S, Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One. 2011;6(9):e24325.PubMedPubMedCentralCrossRef Dinel AL, Andre C, Aubert A, Ferreira G, Laye S, Castanon N. Cognitive and emotional alterations are related to hippocampal inflammation in a mouse model of metabolic syndrome. PLoS One. 2011;6(9):e24325.PubMedPubMedCentralCrossRef
85.
86.
Zurück zum Zitat Kuhad A, Bishnoi M, Tiwari V, Chopra K. Suppression of NF-kappabeta signaling pathway by tocotrienol can prevent diabetes associated cognitive deficits. Pharmacol Biochem Behav. 2009;92(2):251–9.PubMedCrossRef Kuhad A, Bishnoi M, Tiwari V, Chopra K. Suppression of NF-kappabeta signaling pathway by tocotrienol can prevent diabetes associated cognitive deficits. Pharmacol Biochem Behav. 2009;92(2):251–9.PubMedCrossRef
88.
Zurück zum Zitat Sima AA. Encephalopathies: the emerging diabetic complications. Acta Diabetol. 2010;47(4):279–93.PubMedCrossRef Sima AA. Encephalopathies: the emerging diabetic complications. Acta Diabetol. 2010;47(4):279–93.PubMedCrossRef
89.
Zurück zum Zitat Fiatarone Singh MA, Gates N, Saigal N, Wilson GC, Meiklejohn J, Brodaty H, et al. The Study of Mental and Resistance Training (SMART) study-resistance training and/or cognitive training in mild cognitive impairment: a randomized, double-blind, double-sham controlled trial. J Am Med Dir Assoc. 2014;15(12):873–80.PubMedCrossRef Fiatarone Singh MA, Gates N, Saigal N, Wilson GC, Meiklejohn J, Brodaty H, et al. The Study of Mental and Resistance Training (SMART) study-resistance training and/or cognitive training in mild cognitive impairment: a randomized, double-blind, double-sham controlled trial. J Am Med Dir Assoc. 2014;15(12):873–80.PubMedCrossRef
90.
Zurück zum Zitat Guimaraes FC, Amorim PR, Dos Reis FF, Bonoto RT, de Oliveira WC, Moura TA, et al. Physical activity and better medication compliance improve mini-mental state examination scores in the elderly. Dement Geriatr Cogn Disord. 2015;39(1–2):25–31.PubMedCrossRef Guimaraes FC, Amorim PR, Dos Reis FF, Bonoto RT, de Oliveira WC, Moura TA, et al. Physical activity and better medication compliance improve mini-mental state examination scores in the elderly. Dement Geriatr Cogn Disord. 2015;39(1–2):25–31.PubMedCrossRef
91.
Zurück zum Zitat Gates N, Fiatarone Singh MA, Sachdev PS, Valenzuela M. The effect of exercise training on cognitive function in older adults with mild cognitive impairment: a meta-analysis of randomized controlled trials. Am J Geriatr Psychiatry. 2013;21(11):1086–97.PubMedCrossRef Gates N, Fiatarone Singh MA, Sachdev PS, Valenzuela M. The effect of exercise training on cognitive function in older adults with mild cognitive impairment: a meta-analysis of randomized controlled trials. Am J Geriatr Psychiatry. 2013;21(11):1086–97.PubMedCrossRef
92.
Zurück zum Zitat Fiocco AJ, Scarcello S, Marzolini S, Chan A, Oh P, Proulx G, et al. The effects of an exercise and lifestyle intervention program on cardiovascular, metabolic factors and cognitive performance in middle-aged adults with type II diabetes: a pilot study. Can J Diabetes. 2013;37(4):214–9.PubMedCrossRef Fiocco AJ, Scarcello S, Marzolini S, Chan A, Oh P, Proulx G, et al. The effects of an exercise and lifestyle intervention program on cardiovascular, metabolic factors and cognitive performance in middle-aged adults with type II diabetes: a pilot study. Can J Diabetes. 2013;37(4):214–9.PubMedCrossRef
93.
Zurück zum Zitat Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, et al. Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer’s disease. J Alzheimers Dis. 2010;22(2):569–79.PubMedPubMedCentral Baker LD, Frank LL, Foster-Schubert K, Green PS, Wilkinson CW, McTiernan A, et al. Aerobic exercise improves cognition for older adults with glucose intolerance, a risk factor for Alzheimer’s disease. J Alzheimers Dis. 2010;22(2):569–79.PubMedPubMedCentral
94.
Zurück zum Zitat Watson GS, Reger MA, Baker LD, McNeely MJ, Fujimoto WY, Kahn SE, et al. Effects of exercise and nutrition on memory in Japanese Americans with impaired glucose tolerance. Diabetes Care. 2006;29(1):135–6.PubMedCrossRef Watson GS, Reger MA, Baker LD, McNeely MJ, Fujimoto WY, Kahn SE, et al. Effects of exercise and nutrition on memory in Japanese Americans with impaired glucose tolerance. Diabetes Care. 2006;29(1):135–6.PubMedCrossRef
95.
Zurück zum Zitat Ang L, Jaiswal M, Martin C, Pop-Busui R. Glucose control and diabetic neuropathy: lessons from recent large clinical trials. Curr Diab Rep. 2014;14(9):528–0528.PubMedCrossRef Ang L, Jaiswal M, Martin C, Pop-Busui R. Glucose control and diabetic neuropathy: lessons from recent large clinical trials. Curr Diab Rep. 2014;14(9):528–0528.PubMedCrossRef
96.
Zurück zum Zitat Rdzak GM, Abdelghany O. Does insulin therapy for type 1 diabetes mellitus protect against Alzheimer’s disease? Pharmacotherapy. 2014;34(12):1317–23.PubMedCrossRef Rdzak GM, Abdelghany O. Does insulin therapy for type 1 diabetes mellitus protect against Alzheimer’s disease? Pharmacotherapy. 2014;34(12):1317–23.PubMedCrossRef
97.
Zurück zum Zitat Liu W, Li G, Holscher C, Li L. Neuroprotective effects of geniposide on Alzheimer’s disease pathology. Rev Neurosci. 2015;26(4):371–83.PubMed Liu W, Li G, Holscher C, Li L. Neuroprotective effects of geniposide on Alzheimer’s disease pathology. Rev Neurosci. 2015;26(4):371–83.PubMed
98.
Zurück zum Zitat Kosaraju J, Murthy V, Khatwal RB, Dubala A, Chinni S, Muthureddy Nataraj SK, et al. Vildagliptin: an anti-diabetes agent ameliorates cognitive deficits and pathology observed in streptozotocin-induced Alzheimer’s disease. J Pharm Pharmacol. 2013;65(12):1773–84.PubMedCrossRef Kosaraju J, Murthy V, Khatwal RB, Dubala A, Chinni S, Muthureddy Nataraj SK, et al. Vildagliptin: an anti-diabetes agent ameliorates cognitive deficits and pathology observed in streptozotocin-induced Alzheimer’s disease. J Pharm Pharmacol. 2013;65(12):1773–84.PubMedCrossRef
100.
Zurück zum Zitat McClean PL, Parthsarathy V, Faivre E, Holscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer’s disease. J Neurosci. 2011;31(17):6587–94.PubMedCrossRef McClean PL, Parthsarathy V, Faivre E, Holscher C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer’s disease. J Neurosci. 2011;31(17):6587–94.PubMedCrossRef
101.
Zurück zum Zitat Pipatpiboon N, Pintana H, Pratchayasakul W, Chattipakorn N, Chattipakorn SC. DPP4-inhibitor improves neuronal insulin receptor function, brain mitochondrial function and cognitive function in rats with insulin resistance induced by high-fat diet consumption. Eur J Neurosci. 2013;37(5):839–49.PubMedCrossRef Pipatpiboon N, Pintana H, Pratchayasakul W, Chattipakorn N, Chattipakorn SC. DPP4-inhibitor improves neuronal insulin receptor function, brain mitochondrial function and cognitive function in rats with insulin resistance induced by high-fat diet consumption. Eur J Neurosci. 2013;37(5):839–49.PubMedCrossRef
102.
Zurück zum Zitat Pintana H, Apaijai N, Chattipakorn N, Chattipakorn SC. DPP-4 inhibitors improve cognition and brain mitochondrial function of insulin-resistant rats. J Endocrinol. 2013;218(1):1–11.PubMedCrossRef Pintana H, Apaijai N, Chattipakorn N, Chattipakorn SC. DPP-4 inhibitors improve cognition and brain mitochondrial function of insulin-resistant rats. J Endocrinol. 2013;218(1):1–11.PubMedCrossRef
103.
Zurück zum Zitat Kuhad A, Chopra K. Effect of sesamol on diabetes-associated cognitive decline in rats. Exp Brain Res. 2008;185(3):411–20.PubMedCrossRef Kuhad A, Chopra K. Effect of sesamol on diabetes-associated cognitive decline in rats. Exp Brain Res. 2008;185(3):411–20.PubMedCrossRef
104.
Zurück zum Zitat Tuzcu M, Baydas G. Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol. 2006;537(1–3):106–10.PubMedCrossRef Tuzcu M, Baydas G. Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur J Pharmacol. 2006;537(1–3):106–10.PubMedCrossRef
105.
Zurück zum Zitat Kuhad A, Chopra K. Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur J Pharmacol. 2007;576(1–3):34–42.PubMedCrossRef Kuhad A, Chopra K. Curcumin attenuates diabetic encephalopathy in rats: behavioral and biochemical evidences. Eur J Pharmacol. 2007;576(1–3):34–42.PubMedCrossRef
Metadaten
Titel
Diabetes and Cognitive Impairment
verfasst von
Lindsay A. Zilliox
Krish Chadrasekaran
Justin Y. Kwan
James W. Russell
Publikationsdatum
01.09.2016
Verlag
Springer US
Erschienen in
Current Diabetes Reports / Ausgabe 9/2016
Print ISSN: 1534-4827
Elektronische ISSN: 1539-0829
DOI
https://doi.org/10.1007/s11892-016-0775-x

Weitere Artikel der Ausgabe 9/2016

Current Diabetes Reports 9/2016 Zur Ausgabe

Economics and Policy in Diabetes (ES Huang and A Baig, Section Editors)

Diabetes Prevention Interventions in Latin American Countries: a Scoping Review

Psychosocial Aspects (S Jaser and KK Hood, Section Editors)

Physical Activity in Youth With Type 1 Diabetes: a Review

Microvascular Complications—Neuropathy (R Pop-Busui, Section Editor)

Is Stem Cell Transplantation Ready for Prime Time in Diabetic Polyneuropathy?

Treatment of Type 1 Diabetes (M Pietropaolo, Section Editor)

Management of Hypoglycemia in Children and Adolescents with Type 1 Diabetes Mellitus

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.