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Dysregulation of Glycogen Metabolism with Concomitant Spatial Memory Dysfunction in Type 2 Diabetes: Potential Beneficial Effects of Chronic Exercise

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Part of the Advances in Neurobiology book series (NEUROBIOL, volume 23)

Abstract

Cognitive dysfunction is one of the comorbidities of diabetes mellitus, but hippocampus-dependent learning and memory, a component of cognitive function, shows particular decline in type 2 diabetes, suggesting an increased risk for dementia and Alzheimer’s disease. Cognitive function is related to dysregulated glucose metabolism, which is the typical cause of type 2 diabetes; however, hippocampal glycogen and its metabolite lactate are also crucial for hippocampus-dependent memory function. Type 2 diabetes induced hippocampus-dependent learning and memory dysfunction can be improved by chronic exercise and this improvement may possibly mediate through an adaptation of the astrocyte-neuron lactate shuttle (ANLS). This chapter focuses on the dysregulation of hippocampal glycometabolism in type 2 diabetes examining both existing evidence as well as the potential underlying pathophysiological mechanism responsible for memory dysfunction in type 2 diabetes, and showing for the first time that chronic exercise could be an effective therapy for type-2-diabetes-induced hippocampal memory decline.

Keywords

Type 2 diabetes mellitus Hippocampus-dependent learning and memory Hippocampal glycometabolism Monocarboxylate transporter 2 

Abbreviations

ANLS

Astrocyte-neuron lactate shuttle

BDNF

Brain-derived neurotrophic factor

DAB

1,4-Dideoxy-1,4-imino-D-arabinitol

GLUT

Glucose transporter

GSK-3β

Phosphorylated-GS kinase-3β

LETO

Long-Evans Tokushima Otsuka

LTP

Long-term potentiation

MCT

Monocarboxylate transporters

MHPG

NA metabolites

NA

Noradrenaline

NMDA

N-methyl-d-aspartate

OLETF

Otsuka Long-Evans Tokushima Fatty

pCofilin

Phosphorylated-Cofilin

pCREB

Phosphorylated-cAMP-response-element-binding protein

PGK

Phosphoglycerate kinase

PTG

Protein targeting to glycogen

STZ

Streptozotocin

VIP

Vasoactive intestinal peptide

ZDF

Zucker diabetic fatty

ZL

Zucker lean

ZO

Zucker obese

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References

  1. Ahtiluoto S, Polvikoski T, Peltonen M, Solomon A, Tuomilehto J, Winblad B, Sulkava R, Kivipelto M (2010) Diabetes, Alzheimer disease, and vascular dementia: a population-based neuropathologic study. Neurology 75:1195–1202PubMedCrossRefGoogle Scholar
  2. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145PubMedCrossRefGoogle Scholar
  3. Allaman I, Pellerin L, Magistretti PJ (2000) Protein targeting to glycogen mRNA expression is stimulated by noradrenaline in mouse cortical astrocytes. Glia 30:382–391PubMedCrossRefGoogle Scholar
  4. Allaman I, Pellerin L, Magistretti PJ (2003) Glucocorticoids modulate neurotransmitter-induced glycogen metabolism in cultured cortical astrocytes. J Neurochem 88:900–908CrossRefGoogle Scholar
  5. Aveseh M, Nikooie R, Sheibani V, Esmaeili-Mahani S (2014) Endurance training increases brain lactate uptake during hypoglycemia by up regulation of brain lactate transporters. Mol Cell Endocrinol 394:29–36PubMedCrossRefGoogle Scholar
  6. Balducci S, Iacobellis G, Parisi L, Di Biase N, Calandriello E, Leonetti F, Fallucca F (2006) Exercise training can modify the natural history of diabetic peripheral neuropathy. J Diabetes Complications 20:216–223PubMedCrossRefGoogle Scholar
  7. Bélanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14:724–738PubMedCrossRefGoogle Scholar
  8. Bergström J, Hultman E (1966) Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature 210:309–310PubMedCrossRefGoogle Scholar
  9. Bhattacharjee M, Venugopal B, Wong K, Goto Y, Bhattacharjee M (2006) Mitochondrial disorder, diabetes mellitus, and findings in three muscles, including the heart. Ultrastruct Pathol 30:481–487PubMedCrossRefGoogle Scholar
  10. Biessels GJ, Despa F (2018) Cognitive decline and dementia in diabetes mellitus: mechanisms and clinical implications. Nat Rev Endocrinol 14:591–604PubMedPubMedCentralCrossRefGoogle Scholar
  11. Biessels G-J, Kamal A, Ramakers GM, Urban IJ, Spruijt BM, Erkelens DW, Gispen WH (1996) Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45:1259–1266PubMedCrossRefGoogle Scholar
  12. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P (2006) Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 5:64–74PubMedCrossRefGoogle Scholar
  13. Bolz L, Heigele S, Bischofberger J (2015) Running improves pattern separation during novel object recognition. Brain Plast 1:129–141PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boury-Jamot B, Carrad A, Martin J, Halfon O, Magistretti P, Boutrel B (2015) Disrupting astrocyte–neuron lactate transfer persistently reduces conditioned responses to cocaine. Mol Psychiatry 21:1–7Google Scholar
  15. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The arc of synaptic memory. Exp Brain Res 200:125–140PubMedCrossRefGoogle Scholar
  16. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042–2046PubMedCrossRefGoogle Scholar
  17. Canada SE, Weaver SA, Sharpe SN, Pederson BA (2011) Brain glycogen supercompensation in the mouse after recovery from insulin-induced hypoglycemia. J Neurosci Res 89:585–591PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cardinaux JR, Magistretti PJ (1996) Vasoactive intestinal peptide, pituitary adenylate cyclase-activating peptide, and noradrenaline induce the transcription factors CCAAT/enhancer binding protein (C/EBP)-beta and C/EBP delta in mouse cortical astrocytes: involvement in cAMP-regulated glyco. J Neurosci 16:919–929PubMedPubMedCentralCrossRefGoogle Scholar
  19. Caroni P, Donato F, Muller D (2012) Structural plasticity upon learning: regulation and functions. Nat Rev Neurosci 13:478–490PubMedCrossRefGoogle Scholar
  20. Chabot C, Massicotte G, Milot M, Trudeau F, Gagné J (1997) Impaired modulation of AMPA receptors by calcium-dependent processes in streptozotocin-induced diabetic rats. Brain Res 768:249–256PubMedCrossRefGoogle Scholar
  21. Choi IY, Seaquist ER, Gruetter R (2003) Effect of hypoglycemia on brain glycogen metabolism in vivo. J Neurosci Res 72:25–32PubMedPubMedCentralCrossRefGoogle Scholar
  22. Choi HB, Gordon GRJ, Zhou N, Tai C, Rungta RL, Martinez J, Milner TA, Ryu JK, McLarnon JG, Tresguerres M, Levin LR, Buck J, MacVicar BA (2012) Metabolic communication between astrocytes and neurons via bicarbonate-responsive soluble adenylyl Cyclase. Neuron 75:1094–1104PubMedPubMedCentralCrossRefGoogle Scholar
  23. Colberg SR, Sigal RJ, Fernhall B, Regensteiner JG, Blissmer BJ, Rubin RR, Chasan-Taber L, Albright AL, Braun B (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement. Diabetes Care 33:e147–e167PubMedPubMedCentralCrossRefGoogle Scholar
  24. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ (2010) Running enhances spatial pattern separation in mice. Proc Natl Acad Sci 107:2367–2372PubMedCrossRefGoogle Scholar
  25. Crosson SM, Khan A, Printen J, Pessin JE, Saltiel AR (2003) PTG gene deletion causes impaired glycogen synthesis and developmental insulin resistance. J Clin Invest 111:1423–1432PubMedPubMedCentralCrossRefGoogle Scholar
  26. Cukierman T, Gerstein HC, Williamson JD (2005) Cognitive decline and dementia in diabetes - systematic overview of prospective observational studies. Diabetologia 48:2460–2469PubMedCrossRefGoogle Scholar
  27. Dringen R, Gebhardt R, Hamprecht B (1993) Glycogen in astrocytes: possible function as lactate supply for neighboring cells. Brain Res 623:208–214PubMedCrossRefGoogle Scholar
  28. Flood JF, Mooradian AD, Morley JE (1990) Characteristics of learning and memory in streptozocin-induced diabetic mice. Diabetes 39:1391–1398PubMedCrossRefGoogle Scholar
  29. Gaesser GA, Brooks GA (1980) Glycogen repletion following continuous and intermittent exercise to exhaustion. J Appl Physiol Resp Env Ex Physiol 49:722–728Google Scholar
  30. Geroldi C, Frisoni GB, Paolisso G, Bandinelli S, Lamponi M, Abbatecola AM, Zanetti O, Guralnik JM, Ferrucci L (2005) Insulin resistance in cognitive impairment. Arch Neurol 62:1067–1072PubMedCrossRefGoogle Scholar
  31. Gibbs ME, O’Dowd BS, Hertz E, Hertz L (2006) Astrocytic energy metabolism consolidates memory in young chicks. Neuroscience 141:9–13PubMedCrossRefGoogle Scholar
  32. Gispen WH, Biessels GJ (2000) Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23:542–549PubMedCrossRefGoogle Scholar
  33. Gold SM, Dziobek I, Sweat V, Tirsi A, Rogers K, Bruehl H, Tsui W, Richardson S, Javier E, Convit A (2007) Hippocampal damage and memory impairments as possible early brain complications of type 2 diabetes. Diabetologia 50:711–719PubMedCrossRefGoogle Scholar
  34. Gollnick PD, Piehl K, Saltin B (1974) Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol 241:45–57PubMedPubMedCentralCrossRefGoogle Scholar
  35. den Heijer T, Vermeer SE, van Dijk EJ, Prins ND, Koudstaal PJ, Hofman A, Breteler MMB (2003) Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 46:1604–1610CrossRefGoogle Scholar
  36. Hof PR, Pascale E, Magistretti PJ (1988) K+ at concentrations reached in the extracellular space during neuronal activity promotes a Ca2+−dependent glycogen hydrolysis in mouse cerebral cortex. J Neurosci 8:1922–1928PubMedPubMedCentralCrossRefGoogle Scholar
  37. Holloszy JO (2005) Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol 63110:338–343CrossRefGoogle Scholar
  38. James DE, Kraegen EW (1984) The effect of exercise training on glycogen, glycogen synthase and phosphorylase in muscle and liver. Eur J Appl Physiol Occup Physiol 52:276–281PubMedCrossRefGoogle Scholar
  39. Jenkins NT, Padilla J, Arce-Esquivel AA, Bayless DS, Martin JS, Leidy HJ, Booth FW, Rector RS, Laughlin MH (2012) Effects of endurance exercise training, metformin, and their combination on adipose tissue leptin and IL-10 secretion in OLETF rats. J Appl Physiol 113:1873–1883PubMedPubMedCentralCrossRefGoogle Scholar
  40. Juel C, Holten MK, Dela F (2004) Effects of strength training on muscle lactate release and MCT1 and MCT4 content in healthy and type 2 diabetic humans. J Physiol 556:297–304PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kamal A, Biessels GJ, Urban IJGW (1999) Hippocampal synaptic plasticity in streptozotocin-diabetic rats: impairment of long-term potentiation and facilitation of long-term depression. Neuroscience 90:737–745PubMedCrossRefGoogle Scholar
  42. Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T (1992) Spontaneous long-term hyperglycemic rat with diabetic complications. Otsuka long-Evans Tokushima fatty (OLETF) strain. Diabetes 41:1422–1428PubMedCrossRefGoogle Scholar
  43. Kitaoka R, Fujikawa T, Miyaki T, Matsumura S, Fushiki T, Inoue K (2010) Increased noradrenergic activity in the ventromedial hypothalamus during treadmill running in rats. J Nutr Sci Vitaminol (Tokyo) 56:185–190CrossRefGoogle Scholar
  44. Kong J, Shepel PN, Holden CP, Mackiewicz M, Pack AI, Geiger JD (2002) Brain glycogen decreases with increased periods of wakefulness: implications for homeostatic drive to sleep. J Neurosci 22:5581–5587PubMedPubMedCentralCrossRefGoogle Scholar
  45. Lee H, Chang H, Park JY, Kim SY, Choi KM, Song W (2011) Exercise training improves basal blood glucose metabolism with no changes of cytosolic inhibitor κB kinase or c-Jun N-terminal kinase activation in skeletal muscle of Otsuka long-Evans Tokushima fatty rats. Exp Physiol 96:689–698PubMedCrossRefGoogle Scholar
  46. Liu YF, Chen HI, Wu CL, Kuo YM, Yu L, Huang AM, Sen WF, Chuang JI, Jen CJ (2009) Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol 587:3221–3231PubMedPubMedCentralCrossRefGoogle Scholar
  47. Magistretti PJ (2006) Neuron-glia metabolic coupling and plasticity. J Exp Biol 209:2304–2311PubMedCrossRefGoogle Scholar
  48. Magistretti PJ, Pellerin L (1999) Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354:1155–1163PubMedPubMedCentralCrossRefGoogle Scholar
  49. Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE (1981) Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci U S A 78:6535–6539PubMedPubMedCentralCrossRefGoogle Scholar
  50. Manschot SM, Brands AMA, van der Grond J, Kessels RPC, Algra A, Kappelle LJ, Biessels GJ (2006) Brain magnetic resonance imaging correlates of impaired cognition in patients with type 2 diabetes. Diabetes 55:1106–1113PubMedCrossRefGoogle Scholar
  51. Matsui T, Soya S, Okamoto M, Ichitani Y, Kawanaka K, Soya H (2011) Brain glycogen decreases during prolonged exercise. J Physiol 589:3383–3393PubMedPubMedCentralGoogle Scholar
  52. Matsui T, Ishikawa T, Ito H, Okamoto M, Inoue K, Lee MC, Fujikawa T, Ichitani Y, Kawanaka K, Soya H (2012) Brain glycogen supercompensation following exhaustive exercise. J Physiol 590:607–616PubMedCrossRefGoogle Scholar
  53. Matsui T, Soya S, Kawanaka K, Soya H (2015) Brain glycogen decreases during intense exercise without hypoglycemia: the possible involvement of serotonin. Neurochem Res 40:1333–1340PubMedCrossRefGoogle Scholar
  54. Mccrimmon RJ, Phd R, Mccrimmon RJ, Ryan CM, Frier BM (2012) Diabetes and cognitive dysfunction. Lancet 379:2291–2299PubMedCrossRefGoogle Scholar
  55. Mu J, Brozinick JT, Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7:1085–1094PubMedCrossRefGoogle Scholar
  56. Newman LA, Korol DL, Gold PE (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS One 6:e28427PubMedPubMedCentralCrossRefGoogle Scholar
  57. Nikooie R, Rajabi H, Gharakhanlu R, Atabi F, Omidfar K, Aveseh M, Larijani B (2013) Exercise-induced changes of MCT1 in cardiac and skeletal muscles of diabetic rats induced by high-fat diet and STZ. J Physiol Biochem 69:865–877PubMedCrossRefGoogle Scholar
  58. O’Gorman DJ, Karlsson HKR, McQuaid S, Yousif O, Rahman Y, Gasparro D, Glund S, Chibalin AV, Zierath JR, Nolan JJ (2006) Exercise training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein content in patients with type 2 diabetes. Diabetologia 49:2983–2992PubMedCrossRefGoogle Scholar
  59. Ohiwa N, Saito T, Chang H, Omori T, Fujikawa T, Asada T, Soya H (2006) Activation of A1 and A2 noradrenergic neurons in response to running in the rat. Neurosci Lett 395:46–50PubMedCrossRefGoogle Scholar
  60. Ohiwa N, Chang H, Saito T, Onaka T, Fujikawa T, Soya H (2007) Possible inhibitory role of prolactin-releasing peptide for ACTH release associated with running stress. Am J Physiol Regul Integr Comp Physiol 292:R497–R504PubMedCrossRefGoogle Scholar
  61. Pellerin L, Pellegri G, Bittar P, Charnay Y, Bouras C, Martin J, Stella N, Magistretti PJ (1998) Evidence supporting the existence of an activity dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20:291–299PubMedCrossRefGoogle Scholar
  62. Plaschke K, Hoyer S (1993) Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci 11:477–483PubMedCrossRefGoogle Scholar
  63. Pouwer F, Beekman ATF, Nijpels G, Dekker JM, Snoek FJ, Kostense PJ, Heine RJ, Deeg DJH (2003) Rates and risks for co-morbid depression in patients with type 2 diabetes mellitus: results from a community-based study. Diabetologia 46:892–898PubMedCrossRefGoogle Scholar
  64. Ruchti E, Roach PJ, DePaoli-Roach AA, Magistretti PJ, Allaman I (2016) Protein targeting to glycogen is a master regulator of glycogen synthesis in astrocytes. IBRO Rep 1:46–53PubMedPubMedCentralCrossRefGoogle Scholar
  65. Saito T, Soya H (2004) Delineation of responsive AVP-containing neurons to running stress in the hypothalamus. Am J Physiol Regul Integr Comp Physiol 286:R484–R490PubMedCrossRefGoogle Scholar
  66. Secher NH, Seifert T, Van Lieshout JJ (2008) Cerebral blood flow and metabolism during exercise: implications for fatigue. J Appl Physiol 104:306–314PubMedCrossRefGoogle Scholar
  67. Shearer J, Ross KD, Hughey CC, Johnsen VL, Hittel DS, Severson DL (2011) Exercise training does not correct abnormal cardiac glycogen accumulation in the db/db mouse model of type 2 diabetes. Am J Physiol Endocrinol Metab 301:E31–E39PubMedCrossRefGoogle Scholar
  68. Shima T, Jesmin S, Matsui T, Soya M, Soya H (2016a) Differential effects of type 2 diabetes on brain glycometabolism in rats: focus on glycogen and monocarboxylate transporter 2. J Physiol Sci 68:69–75PubMedCrossRefGoogle Scholar
  69. Shima T, Takashi M, Jesmin S, Okamoto M, Soya M, Inoue K, Liu Y-F, Torres-Aleman I, McEwen BS, Soya H (2016b) Moderate exercise ameliorates dysregulated hippocampal glycometabolism and memory function in a rat model of type 2 diabetes. Diabetologia 60:597–606PubMedCrossRefGoogle Scholar
  70. Sickmann HM, Waagepetersen HS, Schousboe A, Benie AJ, Bouman SD (2010) Obesity and type 2 diabetes in rats are associated with altered brain glycogen and amino-acid homeostasis. J Cereb Blood Flow Metab 30:1527–1537PubMedPubMedCentralCrossRefGoogle Scholar
  71. Sickmann HM, Waagepetersen HS, Schousboe A, Benie AJ, Bouman SD (2012) Brain glycogen and its role in supporting glutamate and GABA homeostasis in a type 2 diabetes rat model. Neurochem Int 60:267–275PubMedCrossRefGoogle Scholar
  72. Sigal RJ, Kenny GP, Boule NG, Wells GA, Prud D, Fortier M, Reid RD, Tulloch H, Coyle D, Phillips P, Jennings A, Jaffey J (2007) Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes. Ann Intern Med 147:357–369PubMedCrossRefGoogle Scholar
  73. Soares E, Prediger RD, Nunes S, Castro AA, Viana SD, Lemos C, De Souza CM, Agostinho P, Cunha RA, Carvalho E, Fontes Ribeiro CA, Reis F, Pereira FC (2013) Spatial memory impairments in a prediabetic rat model. Neuroscience 250:565–577PubMedCrossRefGoogle Scholar
  74. Sorg O, Magistretti PJ (1991) Characterization of the glycogenolysis elicited by vasoactive intestinal peptide, noradrenaline and adenosine in primary cultures of mouse cerebral cortical astrocytes. Brain Res 563:227–233PubMedCrossRefGoogle Scholar
  75. Sorg O, Magistretti PJ (1992) Vasoactive intestinal peptide and noradrenaline exert long-term control on glycogen levels in astrocytes: blockade by protein synthesis inhibition. J Neurosci 12:4923–4931PubMedPubMedCentralCrossRefGoogle Scholar
  76. Soya H, Mukai A, Deocaris CC, Ohiwa N, Chang H, Nishijima T, Fujikawa T, Togashi K, Saito T (2007a) Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci Res 58:341–348PubMedPubMedCentralCrossRefGoogle Scholar
  77. Soya H, Nakamura T, Deocaris CC, Kimpara A, Iimura M, Fujikawa T, Chang H, McEwen BS, Nishijima T (2007b) BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 358:961–967PubMedCrossRefGoogle Scholar
  78. Sriwijitkamol A, Coletta DK, Wajcberg E, Balbontin GB, Reyna SM, Barrientes J, Eagan PA, Jenkinson CP, Cersosimo E, DeFronzo RA, Sakamoto K, Musi N (2007) Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study. Diabetes 56:836–848PubMedPubMedCentralCrossRefGoogle Scholar
  79. Stranahan AM (2015) Models and mechanisms for hippocampal dysfunction in obesity and diabetes. Neuroscience 309:125–139PubMedPubMedCentralCrossRefGoogle Scholar
  80. Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler G, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19:951–961PubMedPubMedCentralCrossRefGoogle Scholar
  81. Suge R, Shimazu T, Hasegawa H, Inoue I, Hayashibe H, Nagasaka H, Araki N, Katayama S, Nomura M, Watanabe SI (2012) Cerebral antioxidant enzyme increase associated with learning deficit in type 2 diabetes rats. Brain Res 1481:97–106PubMedCrossRefGoogle Scholar
  82. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–823PubMedPubMedCentralCrossRefGoogle Scholar
  83. Swanson R, Sagar S, Sharp F (1989) Regional brain glycogen stores and metabolism during complete global ischaemia. Neurol Res 11:24–28PubMedCrossRefGoogle Scholar
  84. Swanson RA, Morton MM, Sagar SM, Sharp FR (1992) Sensory stimulation induces local cerebral glycogenolysis: Demonstration by autoradiography. Neuroscience 51:451–461PubMedCrossRefGoogle Scholar
  85. Tekkök S, Krnjevic K (1999) Diabetes mellitus preserves synaptic plasticity in hippocampal slices from middle-age rats. Neuroscience 91:185–191PubMedCrossRefGoogle Scholar
  86. Umegaki H, Hayashi T, Nomura H, Yanagawa M, Nonogaki Z, Nakshima H, Kuzuya M (2013) Cognitive dysfunction: an emerging concept of a new diabetic complication in the elderly. Geriatr Gerontol Int 13:28–34PubMedCrossRefGoogle Scholar
  87. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96:13427–13431PubMedPubMedCentralCrossRefGoogle Scholar
  88. Vissing J, Andersen M, Diemer NH (1996) Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 16:729–736PubMedCrossRefGoogle Scholar
  89. Whitmer RA (2007) Type 2 diabetes and risk of cognitive impairment and dementia. Curr Neurol Neurosci Rep 7:373–380PubMedCrossRefGoogle Scholar
  90. Winder WW, Yang HT, Jaussi AW, Hopkins CR (1987) Epinephrine, glucose, and lactate infusion in exercising adrenodemedullated rats. J Appl Physiol 62:1442–1447PubMedCrossRefGoogle Scholar
  91. Witting A, Chen L, Cudaback E, Straiker A, Walter L, Rickman B, Moller T, Brosnan C, Stella N (2006) Experimental autoimmune encephalomyelitis disrupts endocannabinoid-mediated neuroprotection. Proc Natl Acad Sci 103:6362–6367PubMedCrossRefGoogle Scholar
  92. Yang J, Ruchti E, Petit J-M, Jourdain P, Grenningloh G, Allaman I, Magistretti PJ (2014) Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc Natl Acad Sci U S A 111:12228–12233PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Sport Neuroscience Division, Advanced Research Initiative for Human High Performance (ARIHHP), Faculty of Health and Sport SciencesUniversity of TsukubaTsukubaJapan
  2. 2.Laboratory of Exercise Biochemistry and Neuroendocrinology, Faculty of Health and Sport SciencesUniversity of TsukubaTsukubaJapan

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