Treadmill running improves long-term potentiation (LTP) defects in streptozotocin-induced diabetes at dentate gyrus in rats

Gaven, 1997, Report of the expert committee on the diagnosis and classification of diabetes mellitus, Diabetes Care, 20, 1183, 10.2337/diacare.20.7.1183 Kim, 2003, Treadmill exercise increase cell proliferation in dentate gyrus of rats with streptozotocin-induced diabetes, J. Diabetes Complications, 17, 23, 10.1016/S1056-8727(02)00186-1 Northam, 2009, Central nervous system functions in youth with type 1 diabetes 12 years after disease onset, Diabetes Care, 32, 445, 10.2337/dc08-1657 Biessels, 1996, Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats, Diabetes, 45, 1259, 10.2337/diabetes.45.9.1259 Biessels, 2002, Ageing and diabetes: implications for brain function, Eur. J. Pharmacol., 441, 1, 10.1016/S0014-2999(02)01486-3 Bliss, 1993, Synaptic model of memory: long-term potentiation in the hippocampus, Nature, 361, 31, 10.1038/361031a0 Matthies, 1988, From molecular mechanisms to behavior, Activ. Nerv. Super. (Praha), 30, 2 Artola, 2005, Diabetes mellitus concomitantly facilitates the induction of long term depression and inhibits that of long-term potentiation in hippocampus, Eur. J. Neurosci., 22, 169, 10.1111/j.1460-9568.2005.04205.x Kamal, 2000, Learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: interaction of diabetes and ageing, Diabetologia, 43, 500, 10.1007/s001250051335 Chabot, 1997, Impaired modulatin of AMPA receptors by caclium-dependent processes in streptozotocin-induced diabetic rats, Brain Res., 768, 249, 10.1016/S0006-8993(97)00648-3 Kamal, 1999, Hippocampal synaptic plasticity in streptozotocin-diabetic rats: impairment of long-term potentiation and facilitation of long-term depression, Neuroscience, 90, 737, 10.1016/S0306-4522(98)00485-0 Biessels, 1998, Water maze learning and hippocampal synaptic plasticity in streptozotocin-diabetic rats: effect of insulin treatment, Brain Res., 800, 125, 10.1016/S0006-8993(98)00510-1 Alaei, 2006, Treadmill running reverses retention deficit induced by morphine, Eur. J. Pharmacol., 536, 138, 10.1016/j.ejphar.2006.02.025 Carro, 2001, Circulating insulin-like growth factor I mediated the protective effects of physical exercise against brain insults of different etiology and anatomy, J. Neurosci., 21, 5678, 10.1523/JNEUROSCI.21-15-05678.2001 Tillerson, 2003, Exercise induced behavioral recovery and attenuates neurochemical deficits in rodent models of Parkinson's disease, Neuroscience, 119, 899, 10.1016/S0306-4522(03)00096-4 Farmer, 2004, Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague–Dawley rats in vivo, Neuroscience, 124, 71, 10.1016/j.neuroscience.2003.09.029 O’Callaghan, 2007, The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning, Behav. Brain Res., 176, 362, 10.1016/j.bbr.2006.10.018 Anderson, 2000, Exercise influences spatial learning in the radial arm maze, Physiol. Behav., 70, 425, 10.1016/S0031-9384(00)00282-1 Ang, 2006, Alterations in spatial learning and memory after forced exercise, Brain Res., 1113, 186, 10.1016/j.brainres.2006.07.023 Van praag, 1999, Running enhances neurogenesis, learning and long-term potentation in mice, Proc. Natl. Acad. Sci. U.S.A., 96, 13427, 10.1073/pnas.96.23.13427 Reisi, 2008, Effects of treadmill running on short-term pre-synaptic plasticity at dentate gyrus of streptozotocin-induced diabetic rats, Brain Res., 1211, 30, 10.1016/j.brainres.2008.03.024 Reisi, 2009, Effects of treadmill running on spatial learning and memory in streptozotocin-induced diabetic rats, Neurosci. Lett., 455, 79, 10.1016/j.neulet.2009.03.052 Paxinos, 2005 Lashgari, 2006, Behavioral and electrophysiological studies of chronic oral administration of L-type calcium channel blocker verapamil on learning and memory in rats, Behav. Brain Res., 171, 324, 10.1016/j.bbr.2006.04.013 Kim, 2002, Treadmill exercise increases cell proliferation without altering of apoptosis in dentate gyrus of Sprague–Dawley rats, Life Sci., 71, 1331, 10.1016/S0024-3205(02)01849-0 Uda, 2006, Effects of chronic treadmill running on neurogenesis in the dentate gyrus of the hippocampus of adult rat, Brain Res., 1104, 64, 10.1016/j.brainres.2006.05.066 Johansson, 1996, Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat, Exp. Neurol., 139, 322, 10.1006/exnr.1996.0106 Ohlsson, 1995, Environment influences functional outcome of cerebral infarction in rats, Stroke, 26, 644, 10.1161/01.STR.26.4.644 Sim, 2004, Treadmill exercise improves short-term memory by suppressing ischemia-induced apoptosis of neuronal cells in gerbils, Neurosci. Lett., 372, 256, 10.1016/j.neulet.2004.09.060 Shen, 2001, Physical activity elicits sustained activation of the cyclic AMP response element-binding protein and mitogen-activated protein kinase in the rat hippocampus, Neuroscience, 107, 219, 10.1016/S0306-4522(01)00315-3 Magarinos, 2000, Experimental diabetes in rats causes hippocampal dendritic and synaptic reorganization and increased glucocorticoid reactivity to stress, Proc. Natl. Acad. Sci. U.S.A., 97, 11056, 10.1073/pnas.97.20.11056 Sapolsky, 1992 Lebinger, 1983, Twenty-four-hour cortisol profiles demonstrate exaggerated nocturnal rise in diabetic children, Diabetes Care, 6, 506, 10.2337/diacare.6.5.506 Oster, 1988, Circadian rhythm of corticosterone in diabetic rats, Life Sci., 43, 1643, 10.1016/0024-3205(88)90536-X Revsin, 2009, Glucocorticoid receptor blockade normalizes hippocampal alterations and cognitive impairment in streptozotocin-induced type 1 diabetes mice, Neuropsychopharmacology, 34, 747, 10.1038/npp.2008.136 Munck, 1984, Physiological functions of glucocorticoids in stress and their relation to pharmacological actions, Endocr. Rev., 5, 25, 10.1210/edrv-5-1-25 Filipovic, 2007, The effect of repeated physical exercise on hippocampus and brain cortex in stressed rats, Ann. N. Y. Acad. Sci., 1096, 207, 10.1196/annals.1397.087 Gardoni, 2002, Effects of streptozotocin-diabetes on the hippocampal NMDA receptor complex in the rats, J. Neurochem., 80, 438, 10.1046/j.0022-3042.2001.00713.x Magarinos, 1995, Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors, Neuroscience, 69, 89, 10.1016/0306-4522(95)00259-L Guyot, 2001, The effect of streptozotocin-induced diabetes on the release of excitotoxic and other amino acids from the ischemic rat cerebral cortex, Neurosurgery, 48, 385 Molteni, 2002, Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray, Eur. J. Neurosci., 16, 1107, 10.1046/j.1460-9568.2002.02158.x Gadea, 2001, Glial transporters for glutamate, glycine and GABA. II. Glutamate transporters, J. Neurosci. Res., 63, 453, 10.1002/jnr.1039 Guezennec, 1998, Effects of prolonged exercise on brain ammonia and amino acids, Int. J. Sports Med., 19, 323, 10.1055/s-2007-971925 Holscher, 1998, Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity, Trends Neurosci., 20, 298, 10.1016/S0166-2236(97)01065-5 Zakharenko, 2003, Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1–CA3 synapses, Neuron, 39, 975, 10.1016/S0896-6273(03)00543-9 Ernst, 2000, Stabilization of growing retinal axons by the combined signaling of nitric oxide and brain-derived neurotrophic factor, J. Neurosci., 20, 1458, 10.1523/JNEUROSCI.20-04-01458.2000 Estevez, 1998, Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor, J. Neurosci., 18, 3708, 10.1523/JNEUROSCI.18-10-03708.1998 Reagan, 2002, Diabetes, but not stress, reduces neuronal nitric oxide synthase expression in rat hippocampus: implications for hippocampal synaptic plasticity, Neuroreport, 13, 1801, 10.1097/00001756-200210070-00022 Bonthius, 2003, FGF-2, NGF and IGF-1, but not BDNF, utilize a nitric oxide pathway to signal neurotrophic and neuroprotective effects against alcohol toxicity in cerebellar granule cell cultures, Brain Res. Dev. Brain Res., 140, 15, 10.1016/S0165-3806(02)00549-7 Zhang, 2001, A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats, Ann. Neurol., 50, 602, 10.1002/ana.1249 Endres, 2003, Mechanisms of stroke protection by physical activity, Ann. Neurol., 54, 582, 10.1002/ana.10722