The neuroenergetics of stress hormones in the hippocampus and implications for memory

Frontiers in Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Osborne, D M ^a   Pearson Leary, J ^b   McNay, Ewan C ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; GLUCOSE TRANSPORTER 4; GLUTAMIC ACID; NORADRENALIN; STRESS HORMONE;

CHRONIC STRESS; ENERGY METABOLISM; ENERGY RESOURCE; EXCITOTOXICITY; GLUCOSE METABOLISM; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MEMORY; NEUROMODULATION; NONHUMAN; REVIEW;

EID: 84928671733     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00164     Document Type: Review

References (229)

1. S.I. Sunram-Lea, L. Owen, Y. Finnegan, and H. Hu, Dose-response investigation into glucose facilitation of memory performance and mood in healthy young adults. J Psychopharmacol 25 (2011) 1076-87.
2. E. Baldi, and C. Bucherelli, The inverted "u-shaped" dose-effect relationships in learning and memory: modulation of arousal and consolidation. Nonlinearity in biology, toxicology, medicine 3 (2005) 9-21.
3. L.R. Johnson, J. McGuire, R. Lazarus, and A.A. Palmer, Pavlovian fear memory circuits and phenotype models of PTSD. Neuropharmacology 62 (2012) 638-46.
4. J. Debiec, and J.E. LeDoux, Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Annals of the New York Academy of Sciences 1071 (2006) 521-4.
5. B.M. Elzinga, and J.D. Bremner, Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? Journal of affective disorders 70 (2002) 1-17.
6. M. Fillenz, J.P. Lowry, M.G. Boutelle, and A.E. Fray, The role of astrocytes and noradrenaline in neuronal glucose metabolism. Acta Physiol Scand 167 (1999) 275-84.
7. M.E. Gibbs, D.S. Hutchinson, and R.J. Summers, Role of beta-adrenoceptors in memory consolidation: beta3-adrenoceptors act on glucose uptake and beta2-adrenoceptors on glycogenolysis. Neuropsychopharmacology 33 (2008) 2384-97.
8. R.M. Sapolsky, Glucocorticoid toxicity in the hippocampus: reversal by supplementation with brain fuels. J Neurosci 6 (1986) 2240-4.
9. J.R. Womble, D.F. Larson, J.G. Copeland, B.R. Brown, M.K. Haddox, and D.H. Russell, Adrenal medulla denervation prevents stress-induced epinephrine plasma elevation and cardiac hypertrophy. Life sciences 27 (1980) 2417-20.
10. D.L. Wong, T.C. Tai, D.C. Wong-Faull, R. Claycomb, E.G. Meloni, K.M. Myers, W.A. Carlezon, Jr., and R. Kvetnansky, Epinephrine: a short- and long-term regulator of stress and development of illness: a potential new role for epinephrine in stress. Cell Mol Neurobiol 32 (2012) 737-48.
11. T. Petrov, T.L. Krukoff, and J.H. Jhamandas, Branching projections of catecholaminergic brainstem neurons to the paraventricular hypothalamic nucleus and the central nucleus of the amygdala in the rat. Brain research 609 (1993) 81-92.
12. M.L. Barbaccia, M. Serra, R.H. Purdy, and G. Biggio, Stress and neuroactive steroids. Int Rev Neurobiol 46 (2001) 243-72.
13. J.M. Reul, A. Gesing, S. Droste, I.S. Stec, A. Weber, C. Bachmann, A. Bilang-Bleuel, F. Holsboer, and A.C. Linthorst, The brain mineralocorticoid receptor: greedy for ligand, mysterious in function. Eur J Pharmacol 405 (2000) 235-49.
14. C. Decavel, and A.N. Van den Pol, GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 302 (1990) 1019-37.
15. W.E. Cullinan, GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. The Journal of comparative neurology 419 (2000) 344-51.
16. J.M. Reul, and E.R. de Kloet, Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117 (1985) 2505-11.
17. A. Sarrieau, M. Vial, D. Philibert, M. Moguilewsky, M. Dussaillant, B. McEwen, and W. Rostene, In vitro binding of tritiated glucocorticoids directly on unfixed rat brain sections. Journal of steroid biochemistry 20 (1984) 1233-8.
18. J.M. Reul, and E.R. de Kloet, Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis. Journal of steroid biochemistry 24 (1986) 269-72.
19. J.M. Reul, A. Bilang-Bleuel, S. Droste, A.C. Linthorst, F. Holsboer, and A. Gesing, New mode of hypothalamic-pituitary-adrenocortical axis regulation: significance for stressrelated disorders. Zeitschrift fur Rheumatologie 59 Suppl 2 (2000) II/22-5.
20. J.W. Funder, Corticosteroid hormones and signal specificity. Ann N Y Acad Sci 746 (1994) 1-6; discussion 6-7, 64-7.
21. J.A. Van Eekelen, W. Jiang, E.R. De Kloet, and M.C. Bohn, Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. J Neurosci Res 21 (1988) 88-94.
22. J.P. Herman, P.D. Patel, H. Akil, and S.J. Watson, Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol Endocrinol 3 (1989) 1886-94.
23. M.S. Oitzl, H.M. Reichardt, M. Joels, and E.R. de Kloet, Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 12790-5.
24. S.J. Lupien, C.W. Wilkinson, S. Briere, N.M. Ng Ying Kin, M.J. Meaney, and N.P. Nair, Acute modulation of aged human memory by pharmacological manipulation of glucocorticoids. The Journal of clinical endocrinology and metabolism 87 (2002) 3798-807.
25. S.J. Lupien, C.W. Wilkinson, S. Briere, C. Menard, N.M. Ng Ying Kin, and N.P. Nair, The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 27 (2002) 401-16.
26. L. Cahill, L. Gorski, and K. Le, Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn Mem 10 (2003) 270-4.
27. L. Cahill, and M.T. Alkire, Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiology of learning and memory 79 (2003) 194-8.
28. B. Roozendaal, O. Carmi, and J.L. McGaugh, Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. Proc Natl Acad Sci U S A 93 (1996) 1429-33.
29. M.S. Oitzl, and E.R. de Kloet, Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 106 (1992) 62-71.
30. C. Sandi, and S.P. Rose, Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. The European journal of neuroscience 6 (1994) 1292-7.
31. C. Sandi, and S.P. Rose, Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain research 647 (1994) 106-12.
32. C. Sandi, and S.P. Rose, Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology 133 (1997) 152-60.
33. C. Sandi, M. Loscertales, and C. Guaza, Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. The European journal of neuroscience 9 (1997) 637-42.
34. E.R. de Kloet, M. Joels, and F. Holsboer, Stress and the brain: from adaptation to disease. Nature reviews. Neuroscience 6 (2005) 463-75.
35. B.S. McEwen, Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Annals of the New York Academy of Sciences 933 (2001) 265-77.
36. B. Ferry, and J.L. McGaugh, Clenbuterol administration into the basolateral amygdala posttraining enhances retention in an inhibitory avoidance task. Neurobiology of learning and memory 72 (1999) 8-12.
37. R.T. Lalumiere, and J.L. McGaugh, Memory enhancement induced by post-training intrabasolateral amygdala infusions of beta-adrenergic or muscarinic agonists requires activation of dopamine receptors: Involvement of right, but not left, basolateral amygdala. Learn Mem 12 (2005) 527-32.
38. R.T. LaLumiere, T.V. Buen, and J.L. McGaugh, Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. The Journal of neuroscience: the official journal of the Society for Neuroscience 23 (2003) 6754-8.
39. T. Hatfield, and J.L. McGaugh, Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of learning and memory 71 (1999) 232-9.
40. K.C. Liang, J.L. McGaugh, and H.Y. Yao, Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain research 508 (1990) 225-33.
41. K.C. Liang, and J.L. McGaugh, Lesions of the stria terminalis attenuate the enhancing effect of post-training epinephrine on retention of an inhibitory avoidance response. Behavioural brain research 9 (1983) 49-58.
42. B. Roozendaal, and J.L. McGaugh, Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem 65 (1996) 1-8.
43. K.C. Liang, R.G. Juler, and J.L. McGaugh, Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain research 368 (1986) 125-33.
44. G.L. Quirarte, B. Roozendaal, and J.L. McGaugh, Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 14048-53.
45. B. Roozendaal, B.T. Nguyen, A.E. Power, and J.L. McGaugh, Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci U S A 96 (1999) 11642-7.
46. J.L. McGaugh, The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27 (2004) 1-28.
47. B. Roozendaal, E.L. Hahn, S.V. Nathan, D.J. de Quervain, and J.L. McGaugh, Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J Neurosci 24 (2004) 8161-9.
48. D. Pare, D.R. Collins, and J.G. Pelletier, Amygdala oscillations and the consolidation of emotional memories. Trends in cognitive sciences 6 (2002) 306-314.
49. M.A. Moita, S. Rosis, Y. Zhou, J.E. LeDoux, and H.T. Blair, Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37 (2003) 485-97.
50. R.T. Narayanan, T. Seidenbecher, S. Sangha, O. Stork, and H.C. Pape, Theta resynchronization during reconsolidation of remote contextual fear memory. Neuroreport 18 (2007) 1107-11.
51. H.C. Pape, R.T. Narayanan, J. Smid, O. Stork, and T. Seidenbecher, Theta activity in neurons and networks of the amygdala related to long-term fear memory. Hippocampus 15 (2005) 874-80.
52. T. Seidenbecher, T.R. Laxmi, O. Stork, and H.C. Pape, Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301 (2003) 846-50.
53. J.F. Guzowski, B. Setlow, E.K. Wagner, and J.L. McGaugh, Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate early genes Arc, c-fos, and zif268. The Journal of neuroscience: the official journal of the Society for Neuroscience 21 (2001) 5089-98.
54. T. Miyashita, S. Kubik, N. Haghighi, O. Steward, and J.F. Guzowski, Rapid activation of plasticity-associated gene transcription in hippocampal neurons provides a mechanism for encoding of one-trial experience. J Neurosci 29 (2009) 898-906.
55. A. Vazdarjanova, V. Ramirez-Amaya, N. Insel, T.K. Plummer, S. Rosi, S. Chowdhury, D. Mikhael, P.F. Worley, J.F. Guzowski, and C.A. Barnes, Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498 (2006) 317-29.
56. J.F. Guzowski, B.L. McNaughton, C.A. Barnes, and P.F. Worley, Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2 (1999) 1120-4.
57. J.F. Guzowski, T. Miyashita, M.K. Chawla, J. Sanderson, L.I. Maes, F.P. Houston, P. Lipa, B.L. McNaughton, P.F. Worley, and C.A. Barnes, Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc Natl Acad Sci U S A 103 (2006) 1077-82.
58. C.M. Holloway, and C.K. McIntyre, Post-training disruption of Arc protein expression in the anterior cingulate cortex impairs long-term memory for inhibitory avoidance training. Neurobiol Learn Mem 95 (2011) 425-32.
59. V. Ramirez-Amaya, A. Vazdarjanova, D. Mikhael, S. Rosi, P.F. Worley, and C.A. Barnes, Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25 (2005) 1761-8.
60. A. Vazdarjanova, B.L. McNaughton, C.A. Barnes, P.F. Worley, and J.F. Guzowski, Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J Neurosci 22 (2002) 10067-71.
61. F.C. Yang, and K.C. Liang, Interactions of the dorsal hippocampus, medial prefrontal cortex and nucleus accumbens in formation of fear memory: difference in inhibitory avoidance learning and contextual fear conditioning. Neurobiology of learning and memory 112 (2014) 186-94.
62. P.A. Kabitzke, L. Silva, and C. Wiedenmayer, Norepinephrine mediates contextual fear learning and hippocampal pCREB in juvenile rats exposed to predator odor. Neurobiology of learning and memory 96 (2011) 166-72.
63. K.A. Morris, and P.E. Gold, Age-related impairments in memory and in CREB and pCREB expression in hippocampus and amygdala following inhibitory avoidance training. Mech Ageing Dev 133 (2012) 291-9.
64. A. Stuchlik, T. Petrasek, and K. Vales, A dose-response study of the effects of pre-test administration of beta-adrenergic receptor antagonist propranolol on the learning of active place avoidance, a spatial cognition task, in rats. Behavioural brain research 200 (2009) 144-9.
65. A.L. Mueller, B.J. Hoffer, and T.V. Dunwiddie, Noradrenergic responses in rat hippocampus: evidence for medication by alpha and beta receptors in the in vitro slice. Brain research 214 (1981) 113-26.
66. T. Pearson, and B.G. Frenguelli, Adrenoceptor subtype-specific acceleration of the hypoxic depression of excitatory synaptic transmission in area CA1 of the rat hippocampus. The European journal of neuroscience 20 (2004) 1555-65.
67. D.S. Hutchinson, R.J. Summers, and M.E. Gibbs, Energy metabolism and memory processing: role of glucose transport and glycogen in responses to adrenoceptor activation in the chicken. Brain Res Bull 76 (2008) 224-34.
68. B. Roozendaal, G.K. Hui, I.R. Hui, D.J. Berlau, J.L. McGaugh, and N.M. Weinberger, Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning. Neurobiol Learn Mem 86 (2006) 249-55.
69. J.R. McReynolds, K. Donowho, A. Abdi, J.L. McGaugh, B. Roozendaal, and C.K. McIntyre, Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol Learn Mem 93 (2010) 312-21.
70. B. Ferry, B. Roozendaal, and J.L. McGaugh, Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol Psychiatry 46 (1999) 1140-52.
71. J.L. McGaugh, Making lasting memories: remembering the significant. Proceedings of the National Academy of Sciences of the United States of America 110 Suppl 2 (2013) 10402-7.
72. M. Joels, Corticosteroid effects in the brain: U-shape it. Trends in pharmacological sciences 27 (2006) 244-50.
73. B. Roozendaal, Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of learning and memory 78 (2002) 578-95.
74. C. Kirschbaum, O.T. Wolf, M. May, W. Wippich, and D.H. Hellhammer, Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life sciences 58 (1996) 1475-83.
75. G. Richter-Levin, The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10 (2004) 31-9.
76. B. Roozendaal, Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Prog Neuropsychopharmacol Biol Psychiatry 27 (2003) 1213-23.
77. J. Borrell, E.R. de Kloet, and B. Bohus, Corticosterone decreases the efficacy of adrenaline to affect passive avoidance retention of adrenalectomized rats. Life sciences 34 (1984) 99-104.
78. M. Joels, and E.R. de Kloet, Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 245 (1989) 1502-5.
79. J.A. Polman, E.R. de Kloet, and N.A. Datson, Two populations of glucocorticoid receptorbinding sites in the male rat hippocampal genome. Endocrinology 154 (2013) 1832-44.
80. S.C. Spanswick, J.R. Epp, and R.J. Sutherland, Time-course of hippocampal granule cell degeneration and changes in adult neurogenesis after adrenalectomy in rats. Neuroscience 190 (2011) 166-76.
81. J. Yun, H. Koike, D. Ibi, E. Toth, H. Mizoguchi, A. Nitta, M. Yoneyama, K. Ogita, Y. Yoneda, T. Nabeshima, T. Nagai, and K. Yamada, Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: possible involvement of a brainspecific transcription factor Npas4. Journal of neurochemistry 114 (2010) 1840-51.
82. M. Joels, H. Karst, D. Alfarez, V.M. Heine, Y. Qin, E. van Riel, M. Verkuyl, P.J. Lucassen, and H.J. Krugers, Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7 (2004) 221-31.
83. R.M. Sapolsky, L.C. Krey, and B.S. McEwen, Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. The Journal of neuroscience: the official journal of the Society for Neuroscience 5 (1985) 1222-7.
84. R.M. Sapolsky, Why stress is bad for your brain. Science 273 (1996) 749-50.
85. I.N. Karatsoreos, S.M. Bhagat, N.P. Bowles, Z.M. Weil, D.W. Pfaff, and B.S. McEwen, Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151 (2010) 2117-27.
86. L.P. Reagan, Diabetes as a chronic metabolic stressor: causes, consequences and clinical complications. Exp Neurol 233 (2012) 68-78.
87. S.M. Willi, A. Kennedy, B.P. Brant, P. Wallace, N.L. Rogers, and W.T. Garvey, Effective use of thiazolidinediones for the treatment of glucocorticoid-induced diabetes. Diabetes research and clinical practice 58 (2002) 87-96.
88. L. Ye, F. Wang, and R.H. Yang, Diabetes impairs learning performance and affects the mitochondrial function of hippocampal pyramidal neurons. Brain research 1411 (2011) 57-64.
89. A.M. Stranahan, T.V. Arumugam, R.G. Cutler, K. Lee, J.M. Egan, and M.P. Mattson, Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 11 (2008) 309-17.
90. A. Holmes, and C.L. Wellman, Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33 (2009) 773-83.
91. C. Venero, and J. Borrell, Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. European Journal of Neuroscience 1 (1999) 2465-73.
92. M.Y. Zhu, W.P. Wang, J. Huang, Y.Z. Feng, S. Regunathan, and G. Bissette, Repeated immobilization stress alters rat hippocampal and prefrontal cortical morphology in parallel with endogenous agmatine and arginine decarboxylase levels. Neurochem Int 53 (2008) 346-54.
93. I. Abraham, G. Juhasz, K.A. Kekesi, and K.J. Kovacs, Corticosterone peak is responsible for stress-induced elevation of glutamate in the hippocampus. Stress 2 (1998) 171-81.
94. L. Musazzi, M. Milanese, P. Farisello, S. Zappettini, D. Tardito, V.S. Barbiero, T. Bonifacino, A. Mallei, P. Baldelli, G. Racagni, M. Raiteri, F. Benfenati, G. Bonanno, and M. Popoli, Acute stress increases depolarization-evoked glutamate release in the rat prefrontal/frontal cortex: the dampening action of antidepressants. PLoS One 5 (2010) e8566.
95. A.L. Lussier, R. Romay-Tallon, H.J. Caruncho, and L.E. Kalynchuk, Altered GABAergic and glutamatergic activity within the rat hippocampus and amygdala in rats subjected to repeated corticosterone administration but not restraint stress. Neuroscience 231 (2013) 38-48.
96. E.R. de Kloet, H. Karst, and M. Joels, Corticosteroid hormones in the central stress response: quick-and-slow. Frontiers in neuroendocrinology 29 (2008) 268-72.
97. E.Y. Yuen, W. Liu, I.N. Karatsoreos, Y. Ren, J. Feng, B.S. McEwen, and Z. Yan, Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Molecular psychiatry 16 (2011) 156-70.
98. E.Y. Yuen, W. Liu, I.N. Karatsoreos, J. Feng, B.S. McEwen, and Z. Yan, Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proceedings of the National Academy of Sciences of the United States of America 106 (2009) 14075-9.
99. H. Karst, and M. Joels, Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol 94 (2005) 3479-86.
100. L. Groc, D. Choquet, and F. Chaouloff, The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 11 (2008) 868-70.
101. S. Martin, J.M. Henley, D. Holman, M. Zhou, O. Wiegert, M. van Spronsen, M. Joels, C.C. Hoogenraad, and H.J. Krugers, Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One 4 (2009) e4714.
102. L. Conboy, and C. Sandi, Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action. Neuropsychopharmacology 35 (2010) 674-85.
103. J.J. Harris, R. Jolivet, and D. Attwell, Synaptic energy use and supply. Neuron 75 (2012) 762-77.
104. D. Attwell, and S.B. Laughlin, An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21 (2001) 1133-45.
105. L. Hertz, Glutamate, a neurotransmitter--and so much more. A synopsis of Wierzba III. Neurochem Int 48 (2006) 416-25.
106. M.E. Gibbs, D. Hutchinson, and L. Hertz, Astrocytic involvement in learning and memory consolidation. Neurosci Biobehav Rev 32 (2008) 927-44.
107. L. Hertz, J. Xu, and L. Peng, Glycogenolysis and purinergic signaling. Advances in neurobiology 11 (2014) 31-54.
108. L. Hertz, J. Xu, D. Song, T. Du, B. Li, E. Yan, and L. Peng, Astrocytic glycogenolysis: mechanisms and functions. Metabolic brain disease 30 (2015) 317-33.
109. G. Pagano, P. Cavallo-Perin, M. Cassader, A. Bruno, A. Ozzello, P. Masciola, A.M. Dall'omo, and B. Imbimbo, An in vivo and in vitro study of the mechanism of prednisoneinduced insulin resistance in healthy subjects. The Journal of clinical investigation 72 (1983) 1814-20.
110. M. McMahon, J. Gerich, and R. Rizza, Effects of glucocorticoids on carbohydrate metabolism. Diabetes/metabolism reviews 4 (1988) 17-30.
111. T. Battelino, M. Goto, and W.P. Zeller, Dexamethasone attenuates hypoglycemia in ten day old rats treated with TNF alpha. Research communications in molecular pathology and pharmacology 92 (1996) 149-54.
112. H. Sakoda, T. Ogihara, M. Anai, M. Funaki, K. Inukai, H. Katagiri, Y. Fukushima, Y. Onishi, H. Ono, M. Fujishiro, M. Kikuchi, Y. Oka, and T. Asano, Dexamethasone-induced insulin resistance in 3T3-L1 adipocytes is due to inhibition of glucose transport rather than insulin signal transduction. Diabetes 49 (2000) 1700-8.
113. N. Oda, A. Nakai, T. Mokuno, Y. Sawai, Y. Nishida, T. Mano, K. Asano, Y. Itoh, M. Kotake, S. Kato, and et al., Dexamethasone-induced changes in glucose transporter 4 in rat heart muscle, skeletal muscle and adipocytes. European journal of endocrinology/European Federation of Endocrine Societies 133 (1995) 121-6.
114. W.T. Garvey, T.P. Huecksteadt, R. Monzon, and S. Marshall, Dexamethasone regulates the glucose transport system in primary cultured adipocytes: different mechanisms of insulin resistance after acute and chronic exposure. Endocrinology 124 (1989) 2063-73.
115. S. Mohseni, Neurologic damage in hypoglycemia. Handbook of clinical neurology 126 (2014) 513-32.
116. E.V. Stelmashook, E.R. Lozier, E.S. Goryacheva, P. Mergenthaler, S.V. Novikova, D.B. Zorov, and N.K. Isaev, Glutamine-mediated protection from neuronal cell death depends on mitochondrial activity. Neuroscience letters 482 (2010) 151-5.
117. G.R. Sutherland, R.L. Tyson, and R.N. Auer, Truncation of the krebs cycle during hypoglycemic coma. Med Chem 4 (2008) 379-85.
118. K. Hernandez-Fonseca, N. Cardenas-Rodriguez, J. Pedraza-Chaverri, and L. Massieu, Calcium-dependent production of reactive oxygen species is involved in neuronal damage induced during glycolysis inhibition in cultured hippocampal neurons. Journal of neuroscience research 86 (2008) 1768-80.
119. L.J. Martin, N.A. Al-Abdulla, A.M. Brambrink, J.R. Kirsch, F.E. Sieber, and C. Portera- Cailliau, Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: A perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46 (1998) 281-309.
120. M.P. Mattson, Neuroprotective signal transduction: relevance to stroke. Neurosci Biobehav Rev 21 (1997) 193-206.
121. A. Camacho, and L. Massieu, Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Archives of medical research 37 (2006) 11-8.
122. P.E. Gold, Glucose modulation of memory storage processing. Behav Neural Biol 45 (1986) 342-9.
123. M.K. Lee, S.N. Graham, and P.E. Gold, Memory enhancement with posttraining intraventricular glucose injections in rats. Behav Neurosci 102 (1988) 591-5.
124. D.L. Krebs, and M.B. Parent, The enhancing effects of hippocampal infusions of glucose are not restricted to spatial working memory. Neurobiology of learning and memory 83 (2005) 168-72.
125. A. Suzuki, S.A. Stern, O. Bozdagi, G.W. Huntley, R.H. Walker, P.J. Magistretti, and C.M. Alberini, Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144 (2011) 810-23.
126. C. Messier, Glucose improvement of memory: a review. European journal of pharmacology 490 (2004) 33-57.
127. D.L. Korol, and P.E. Gold, Glucose, memory, and aging. Am J Clin Nutr 67 (1998) 764S- 771S.
128. S.M. de la Monte, Brain insulin resistance and deficiency as therapeutic targets in Alzheimer's disease. Curr Alzheimer Res 9 (2012) 35-66.
129. N. Moroz, M. Tong, L. Longato, H. Xu, and S.M. de la Monte, Limited Alzheimer-type neurodegeneration in experimental obesity and type 2 diabetes mellitus. J Alzheimers Dis 15 (2008) 29-44.
130. E.C. McNay, T.M. Fries, and P.E. Gold, Decreases in rat extracellular hippocampal glucose concentration associated with cognitive demand during a spatial task. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 2881-5.
131. V. Job, G.M. Walton, K. Bernecker, and C.S. Dweck, Beliefs about willpower determine the impact of glucose on self-control. Proceedings of the National Academy of Sciences of the United States of America 110 (2013) 14837-42.
132. M.T. Gailliot, and R.F. Baumeister, The physiology of willpower: linking blood glucose to self-control. Personality and social psychology review: an official journal of the Society for Personality and Social Psychology, Inc 11 (2007) 303-27.
133. M.T. Gailliot, R.F. Baumeister, C.N. DeWall, J.K. Maner, E.A. Plant, D.M. Tice, L.E. Brewer, and B.J. Schmeichel, Self-control relies on glucose as a limited energy source: willpower is more than a metaphor. J Pers Soc Psychol 92 (2007) 325-36.
134. L.A. Sandusky, R.W. Flint, and E.C. McNay, Elevated glucose metabolism in the amygdala during an inhibitory avoidance task. Behav Brain Res 245 (2013) 83-7.
135. E.C. McNay, and P.E. Gold, Food for thought: fluctuations in brain extracellular glucose provide insight into the mechanisms of memory modulation. Cognitive and Behavioural Neuroscience Reviews 1 (2002) 264-280.
136. C.S. Roy, and C.S. Sherrington, On the Regulation of the Blood-supply of the Brain. J Physiol 11 (1890) 85-158 17.
137. L. Pellerin, G. Pellegri, P.G. Bittar, Y. Charnay, C. Bouras, J.L. Martin, N. Stella, and P.J. Magistretti, Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 20 (1998) 291-9.
138. L. Pellerin, A.K. Bouzier-Sore, A. Aubert, S. Serres, M. Merle, R. Costalat, and P.J. Magistretti, Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55 (2007) 1251-62.
139. J.N. Livingston, and D.H. Lockwood, Effect of glucocorticoids on the glucose transport system of isolated fat cells. The Journal of biological chemistry 250 (1975) 8353-60.
140. C. Weissman, The metabolic response to stress: an overview and update. Anesthesiology 73 (1990) 308-27.
141. L.A. De Bruin, E.M. Schasfoort, A.B. Steffens, and J. Korf, Effects of stress and exercise on rat hippocampus and striatum extracellular lactate. The American journal of physiology 259 (1990) R773-9.
142. W.P. Borg, R.S. Sherwin, M.J. During, M.A. Borg, and G.I. Shulman, Local ventromedial hypothalamus glucopenia triggers counterregulatory hormone release. Diabetes 44 (1995) 180-4.
143. M.A. Borg, R.S. Sherwin, W.P. Borg, W.V. Tamborlane, and G.I. Shulman, Local ventromedial hypothalamus glucose perfusion blocks counterregulation during systemic hypoglycemia in rats. J Clin Invest 99 (1997) 361-5.
144. M. Borg, W. Tamborlane, G. Shulman, and R. Sherwin, Local lactate perfusion of the ventromedial hypothalamus suppresses hypoglycemic counterregulation. Diabetes (2003) (in press).
145. R.P. Hoffman, Sympathetic mechanisms of hypoglycemic counterregulation. Curr Diabetes Rev 3 (2007) 185-93.
146. E.M. Schasfoort, L.A. De Bruin, and J. Korf, Mild stress stimulates rat hippocampal glucose utilization transiently via NMDA receptors, as assessed by lactography. Brain research 475 (1988) 58-63.
147. A. Munck, Glucocorticoid inhibition of glucose uptake by peripheral tissues: old and new evidence, molecular mechanisms, and physiological significance. Perspectives in biology and medicine 14 (1971) 265-9.
148. L. Zyskowski, and A. Munck, Kinetic studies on the mechanism of glucocorticoid inhibition of hexose transport in rat thymocytes. Journal of steroid biochemistry 10 (1979) 573-9.
149. I.A. Silver, and M. Erecinska, Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J Neurosci 14 (1994) 5068-76.
150. E.C. McNay, and R.S. Sherwin, Effect of recurrent hypoglycemia on spatial cognition and cognitive metabolism in normal and diabetic rats. Diabetes 53 (2004) 418-25.
151. R.L. Martin, H.G. Lloyd, and A.I. Cowan, The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends in neurosciences 17 (1994) 251-7.
152. M. Popoli, Z. Yan, B.S. McEwen, and G. Sanacora, The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nature reviews. Neuroscience 13 (2012) 22-37.
153. H.J. Krugers, D. Jaarsma, and J. Korf, Rat hippocampal lactate efflux during electroconvulsive shock or stress is differently dependent on entorhinal cortex and adrenal integrity. Journal of neurochemistry 58 (1992) 826-30.
154. L.K. Fellows, M.G. Boutelle, and M. Fillenz, Physiological stimulation increases nonoxidative glucose metabolism in the brain of the freely moving rat. Journal of neurochemistry 60 (1993) 1258-63.
155. L. Hertz, L. Peng, and G.A. Dienel, Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 27 (2007) 219-49.
156. L.A. Newman, D.L. Korol, and P.E. Gold, Lactate produced by glycogenolysis in astrocytes regulates memory processing. PLoS One 6 (2011) e28427.
157. I. Allaman, M. Belanger, and P.J. Magistretti, Astrocyte-neuron metabolic relationships: for better and for worse. Trends in neurosciences 34 (2011) 76-87.
158. P.J. Magistretti, and L. Pellerin, Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. Philos Trans R Soc Lond B Biol Sci 354 (1999) 1155-63.
159. L. Pellerin, G. Pellegri, P. Bittar, Y. Charnay, C. Bouras, J. Martin, N. Stella, and P. Magistretti, Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Developmental Neuroscience 20 (1998) 291-299.
160. A.K. Bouzier-Sore, P. Voisin, P. Canioni, P.J. Magistretti, and L. Pellerin, Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 23 (2003) 1298-306.
161. J. Ros, L. Pellerin, F. Magara, J. Dauguet, F. Schenk, and P.J. Magistretti, Metabolic activation pattern of distinct hippocampal subregions during spatial learning and memory retrieval. J Cereb Blood Flow Metab 26 (2005) 468-477.
162. M.T. Wyss, R. Jolivet, A. Buck, P.J. Magistretti, and B. Weber, In Vivo Evidence for Lactate as a Neuronal Energy Source. The Journal of Neuroscience 31 (2011) 7477-7485.
163. G.K. Gandhi, N.F. Cruz, K.K. Ball, and G.A. Dienel, Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons. Journal of neurochemistry 111 (2009) 522-36.
164. G.A. Dienel, Astrocytic energetics during excitatory neurotransmission: What are contributions of glutamate oxidation and glycolysis? Neurochem Int 63 (2013) 244-58.
165. L. Hertz, M.E. Gibbs, and G.A. Dienel, Fluxes of lactate into, from, and among gap junction-coupled astrocytes and their interaction with noradrenaline. Frontiers in neuroscience 8 (2014) 261.
166. M.E. Gibbs, H.G. Lloyd, T. Santa, and L. Hertz, Glycogen is a preferred glutamate precursor during learning in 1-day-old chick: biochemical and behavioral evidence. Journal of neuroscience research 85 (2007) 3326-33.
167. P.E. Gold, Regulation of memory - from the adrenal medulla to liver to astrocytes to neurons. Brain Res Bull 105 (2014) 25-35.
168. T. Miyashita, and C.L. Williams, Epinephrine administration increases neural impulses propagated along the vagus nerve: Role of peripheral beta-adrenergic receptors. Neurobiol Learn Mem 85 (2006) 116-24.
169. T. Miyashita, and C.L. Williams, Peripheral arousal-related hormones modulate norepinephrine release in the hippocampus via influences on brainstem nuclei. Behav Brain Res 153 (2004) 87-95.
170. D.L. Hassert, T. Miyashita, and C.L. Williams, The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav Neurosci 118 (2004) 79-88.
171. T. Miyashita, and C.L. Williams, Enhancement of noradrenergic neurotransmission in the nucleus of the solitary tract modulates memory storage processes. Brain Res 987 (2003) 164-75.
172. T. Miyashita, and C.L. Williams, Glutamatergic transmission in the nucleus of the solitary tract modulates memory through influences on amygdala noradrenergic systems. Behav Neurosci 116 (2002) 13-21.
173. D.F. Pena, J.E. Childs, S. Willett, A. Vital, C.K. McIntyre, and S. Kroener, Vagus nerve stimulation enhances extinction of conditioned fear and modulates plasticity in the pathway from the ventromedial prefrontal cortex to the amygdala. Front Behav Neurosci 8 (2014) 327.
174. D.F. Pena, N.D. Engineer, and C.K. McIntyre, Rapid remission of conditioned fear expression with extinction training paired with vagus nerve stimulation. Biol Psychiatry 73 (2013) 1071-7.
175. B. Ferry, P.J. Magistretti, and E. Pralong, Noradrenaline modulates glutamate-mediated neurotransmission in the rat basolateral amygdala in vitro. The European journal of neuroscience 9 (1997) 1356-64.
176. T. Tajima, H. Endo, Y. Suzuki, H. Ikari, M. Gotoh, and A. Iguchi, Immobilization stressinduced increase of hippocampal acetylcholine and of plasma epinephrine, norepinephrine and glucose in rats. Brain research 720 (1996) 155-8.
177. H. Hourani, D.B. Lacy, T.M. Nammour, N.N. Abumrad, and J.A. Morris, Differential effects of alpha and beta adrenergic blockade on glucose and lactate metabolism during acute stress. The Journal of trauma 30 (1990) 1116-23; discussion 1123-4.
178. C.C. Hsu, and C.S. Hsu, Effect of isoproterenol on the uptake of [14C]glucose into glial cells. Neuroscience research 9 (1990) 54-8.
179. K.V. Subbarao, and L. Hertz, Effect of adrenergic agonists on glycogenolysis in primary cultures of astrocytes. Brain research 536 (1990) 220-6.
180. C.M. Gam, P. Rasmussen, N.H. Secher, T. Seifert, F.S. Larsen, and H.B. Nielsen, Maintained cerebral metabolic ratio during exercise in patients with beta-adrenergic blockade. Clinical physiology and functional imaging 29 (2009) 420-6.
181. J.O. Woods, Long-acting or conventional propanolol in hypertension? The Practitioner 223 (1979) 834-7.
182. R. Arauco, and A. Alagon, [Propanolol in arterial hypertension. Beta-blockaders. Recent advances]. La Prensa medica mexicana 44 (1979) 97-104.
183. C. Grillon, J. Cordova, C.A. Morgan, D.S. Charney, and M. Davis, Effects of the betablocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology (Berl) 175 (2004) 342-52.
184. F. Taherian, A.A. Vafaei, G.H. Vaezi, S. Eskandarian, A. Kashef, and A. Rashidy-Pour, Propranolol-induced Impairment of Contextual Fear Memory Reconsolidation in Rats: A similar Effect on Weak and Strong Recent and Remote Memories. Basic and clinical neuroscience 5 (2014) 231-9.
185. H. Sun, Y. Mao, J. Wang, and Y. Ma, Effects of beta-adrenergic antagonist, propranolol on spatial memory and exploratory behavior in mice. Neurosci Lett 498 (2011) 133-7.
186. A.M. Schneider, P.E. Simson, R.K. Atapattu, and L.G. Kirby, Stress-dependent impairment of passive-avoidance memory by propranolol or naloxone. Pharmacol Biochem Behav 98 (2011) 539-43.
187. N.Y. Oei, M.S. Tollenaar, B.M. Elzinga, and P. Spinhoven, Propranolol reduces emotional distraction in working memory: a partial mediating role of propranolol-induced cortisol increases? Neurobiol Learn Mem 93 (2010) 388-95.
188. E.P. Lim, V. Verma, R. Nagarajah, and G.S. Dawe, Propranolol blocks chronic risperidone treatment-induced enhancement of spatial working memory performance of rats in a delayed matching-to-place water maze task. Psychopharmacology (Berl) 191 (2007) 297-310.
189. I.B. Introini-Collison, A.H. Nagahara, and J.L. McGaugh, Memory enhancement with intraamygdala post-training naloxone is blocked by concurrent administration of propranolol. Brain Res 476 (1989) 94-101.
190. D.B. Sternberg, P.E. Gold, and J.L. McGaugh, Memory facilitation and impairment with supraseizure electrical brain stimulation: attenuation with pretrial propranolol injections. Behav Neural Biol 38 (1983) 261-8.
191. M. Omatsu-Kanbe, and H. Kitasato, Insulin and noradrenaline independently stimulate the translocation of glucose transporters from intracellular stores to the plasma membrane in mouse brown adipocytes. FEBS letters 314 (1992) 246-50.
192. Y. Shimizu, S. Satoh, H. Yano, Y. Minokoshi, S.W. Cushman, and T. Shimazu, Effects of noradrenaline on the cell-surface glucose transporters in cultured brown adipocytes: novel mechanism for selective activation of GLUT1 glucose transporters. The Biochemical journal 330 (Pt 1) (1998) 397-403.
193. S.J. Vannucci, R.R. Clark, E. Koehler-Stec, K. Li, C.B. Smith, P. Davies, F. Maher, and I.A. Simpson, Glucose transporter expression in brain: relationship to cerebral glucose utilization. Dev Neurosci 20 (1998) 369-79.
194. S. El Messari, A. Aït-Ikhlef, D.-H. Ambroise, L. Penicaud, and M. Arluison, Expression of insulin-responsive glucose transporter GLUT4 mRNA in the rat brain and spinal cord: An in situ hybridization study. Journal of Chemical Neuroanatomy 24 (2002) 225-242.
195. J.S. Bogan, and K.V. Kandor, Biogenesis and regulation of insulin-responsive vesicles containing GLUT4. (2010).
196. J. Pearson-Leary, Functional roles for GluT4 in hippocampal memory processing, Psychology, University at Albany, 2013.
197. E.O. Ojuka, V. Goyaram, and J.A. Smith, The role of CaMKII in regulating GLUT4 expression in skeletal muscle. Am J Physiol Endocrinol Metab 303 (2012) E322-31.
198. J. Hertel, H. Struthers, C.B. Horj, and P.W. Hruz, A structural basis for the acute effects of HIV protease inhibitors on GLUT4 intrinsic activity. The Journal of biological chemistry 279 (2004) 55147-52.
199. S. Kristiansen, J. Youn, and E.A. Richter, Effect of vanadate on glucose transporter (GLUT4) intrinsic activity in skeletal muscle plasma membrane giant vesicles. Biochimica et biophysica acta 1282 (1996) 71-5.
200. H. Alkhateeb, A. Chabowski, J.F. Glatz, J.F. Luiken, and A. Bonen, Two phases of palmitate-induced insulin resistance in skeletal muscle: impaired GLUT4 translocation is followed by a reduced GLUT4 intrinsic activity. American journal of physiology. Endocrinology and metabolism 293 (2007) E783-93.
201. E. Uemura, and H.W. Greenlee, Insulin regulates neuronal glucose uptake by promoting translocation of glucose transporter GluT3. Experimental Neurology 198 (2006) 48-53.
202. N. Dehvari, D.S. Hutchinson, J. Nevzorova, O.S. Dallner, M. Sato, M. Kocan, J. Merlin, B.A. Evans, R.J. Summers, and T. Bengtsson, beta(2)-Adrenoceptors increase translocation of GLUT4 via GPCR kinase sites in the receptor C-terminal tail. Br J Pharmacol 165 (2012) 1442-56.
203. M.M. Zanquetta, M.E. Nascimento, R.C. Mori, B. D'Agord Schaan, M.E. Young, and U.F. Machado, Participation of beta-adrenergic activity in modulation of GLUT4 expression during fasting and refeeding in rats. Metabolism: clinical and experimental 55 (2006) 1538-45.
204. B.S. McEwen, and L.P. Reagan, Glucose transporter expression in the central nervous system: relationship to synaptic function. European journal of pharmacology 490 (2004) 13-24.
205. K. Bakirtzi, G. Belfort, I. Lopez-Coviella, D. Kuruppu, L. Cao, E.D. Abel, A.L. Brownell, and K.V. Kandror, Cerebellar neurons possess a vesicular compartment structurally and functionally similar to Glut4-storage vesicles from peripheral insulin-sensitive tissues. J Neurosci 29 (2009) 5193-201.
206. D. Attwell, and A. Gibb, Neuroenergetics and the kinetic design of excitatory synapses. Nat Rev Neurosci 6 (2005) 841-9.
207. M. Kadekaro, M. Ito, and P.M. Gross, Local cerebral glucose utilization is increased in acutely adrenalectomized rats. Neuroendocrinology 47 (1988) 329-34.
208. C.E. Virgin, Jr., T.P. Ha, D.R. Packan, G.C. Tombaugh, S.H. Yang, H.C. Horner, and R.M. Sapolsky, Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem 57 (1991) 1422-8.
209. H.C. Horner, D.R. Packan, and R.M. Sapolsky, Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology 52 (1990) 57-64.
210. L.P. Reagan, Glucose, stress, and hippocampal neuronal vulnerability. International review of neurobiology 51 (2002) 289-324.
211. G.G. Piroli, C.A. Grillo, L.R. Reznikov, S. Adams, B.S. McEwen, M.J. Charron, and L.P. Reagan, Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology 85 (2007) 71-80.
212. A.K. Cherian, and K.P. Briski, Effects of adrenalectomy on neuronal substrate fuel transporter and energy transducer gene expression in hypothalamic and hindbrain metabolic monitoring sites. Neuroendocrinology 91 (2010) 56-63.
213. L.P. Reagan, A.M. Magarinos, L.R. Lucas, A. van Bueren, A.L. McCall, and B.S. McEwen, Regulation of GLUT-3 glucose transporter in the hippocampus of diabetic rats subjected to stress. The American journal of physiology 276 (1999) E879-86.
214. S. Jeyaraj, C. Boehmer, F. Lang, and M. Palmada, Role of SGK1 kinase in regulating glucose transport via glucose transporter GLUT4. Biochem Biophys Res Commun 356 (2007) 629-35.
215. S.P. Weinstein, T. Paquin, A. Pritsker, and R.S. Haber, Glucocorticoid-induced insulin resistance: dexamethasone inhibits the activation of glucose transport in rat skeletal muscle by both insulin- and non-insulin-related stimuli. Diabetes 44 (1995) 441-5.
216. R.C. Andrews, and B.R. Walker, Glucocorticoids and insulin resistance: old hormones, new targets. Clin Sci (Lond) 96 (1999) 513-23.
217. E.C. McNay, C.T. Ong, R.J. McCrimmon, J. Cresswell, J.S. Bogan, and R.S. Sherwin, Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem 93 (2010) 546-53.
218. J. Pearson-Leary, and E.C. McNay, Intrahippocampal administration of amyloid-beta(1-42) oligomers acutely impairs spatial working memory, insulin signaling, and hippocampal metabolism. J Alzheimers Dis 30 (2012) 413-22.
219. M.C. Morsink, P.J. Steenbergen, J.B. Vos, H. Karst, M. Joels, E.R. De Kloet, and N.A. Datson, Acute activation of hippocampal glucocorticoid receptors results in different waves of gene expression throughout time. Journal of neuroendocrinology 18 (2006) 239-52.
220. M.S. Lawrence, and R.M. Sapolsky, Glucocorticoids accelerate ATP loss following metabolic insults in cultured hippocampal neurons. Brain research 646 (1994) 303-6.
221. P.G. Bittar, Y. Charnay, L. Pellerin, C. Bouras, and P.J. Magistretti, Selective distribution of lactate dehydrogenase isoenzymes in neurons and astrocytes of human brain. J Cereb Blood Flow Metab 16 (1996) 1079-89.
222. O. Elekes, K. Venema, F. Postema, R. Dringen, B. Hamprecht, and J. Korf, Evidence that stress activates glial lactate formation in vivo assessed with rat hippocampus lactography. Neuroscience letters 208 (1996) 69-72.
223. J. Korf, Intracerebral trafficking of lactate in vivo during stress, exercise, electroconvulsive shock and ischemia as studied with microdialysis. Developmental neuroscience 18 (1996) 405-14.
224. O. Elekes, K. Venema, F. Postema, R. Dringen, B. Hamprecht, and J. Korf, Possible glial contribution of rat hippocampus lactate as assessed with microdialysis and stress. Acta neurochirurgica. Supplement 67 (1996) 1-5.
225. M. Roy, and R.M. Sapolsky, The exacerbation of hippocampal excitotoxicity by glucocorticoids is not mediated by apoptosis. Neuroendocrinology 77 (2003) 24-31.
226. A.M. Vincent, J.A. Olzmann, M. Brownlee, W.I. Sivitz, and J.W. Russell, Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 53 (2004) 726-34.
227. A. Duarte, T. Proenca, C. Oliviera, M. Santos, and A. Rego, Insulin restores metabolic function in cutured cortical neurons subjected to oxidative stress. Diabetes 55 (2006) 2863-2870.
228. K. Maiese, Z.Z. Chong, and Y.C. Shang, Mechanistic insights into diabetes mellitus and oxidative stress. Current Medicinal Chemistry 14 (2007) 1729-38.
229. C.D. Conrad, Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev Neurosci 19 (2008) 395-411.