Exercise improves recognition memory and synaptic plasticity in the prefrontal cortex for rats modelling vascular dementia

References

• O’Brien JT, Thomas A. Vascular dementia. Lancet. 2015;386:1698–1706.10.1016/S0140-6736(15)00463-8
   PubMed Web of Science ®Google Scholar
• Versijpt J. Effectiveness and cost-effectiveness of the pharmacological treatment of Alzheimer’s disease and vascular dementia. J Alzheimers Dis. 2014;42:S19–25.
   PubMed Web of Science ®Google Scholar
• Bahar-Fuchs A, Clare L, Woods B. Cognitive training and cognitive rehabilitation for persons with mild to moderate dementia of the Alzheimer’s or vascular type: A review. Alzheimers Res Ther. 2013;5(4):35. eCollection. doi:10.1186/alzrt189.
   PubMed Web of Science ®Google Scholar
• Lin Y, Dong J, Yan T, et al. Involuntary, forced and voluntary exercises are equally capable of inducing hippocampal plasticity and the recovery of cognitive function after stroke. Neurol Res. 2015;37:893–901.10.1179/1743132815Y.0000000074
   PubMed Web of Science ®Google Scholar
• Lin Y, Lu X, Dong J, et al. Involuntary, forced and voluntary exercises equally attenuate neurocognitive deficits in vascular dementia by the BDNF-pCREB mediated pathway. Neurochem Res. 2015;40:1839–1848.10.1007/s11064-015-1673-3
   PubMed Web of Science ®Google Scholar
• Stranahan AM, Khalil D, Gould E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus. 2007;17:1017–1022.10.1002/(ISSN)1098-1063
   PubMed Web of Science ®Google Scholar
• Bolduc V, Thorin-Trescases N, Thorin E. Endothelium-dependent control of cerebrovascular functions through age: exercise for healthy cerebrovascular aging. Am J Physiol Heart Circ Physiol. 2013;305:H620–H633.10.1152/ajpheart.00624.2012
   PubMed Web of Science ®Google Scholar
• Popović DB. Advances in functional electrical stimulation (FES). J Electromyogr Kinesiol. 2014;24:795–802.10.1016/j.jelekin.2014.09.008
   PubMed Web of Science ®Google Scholar
• Yan T, Hui-Chan CW, Li LS. Functional electrical stimulation improves motor recovery of the lower extremity and walking ability of subjects with first acute stroke: A randomized placebo-controlled trial. Stroke. 2005;36:80–85.10.1161/01.STR.0000149623.24906.63
   PubMed Web of Science ®Google Scholar
• Tan Z, Liu H, Yan T, et al. The effectiveness of functional electrical stimulation based on a normal gait pattern on subjects with early stroke: A randomized controlled trial. BioMed Res Int. 2014;7:1–9.
   Google Scholar
• You G, Liang H, Yan T. Functional electrical stimulation early after stroke improves lower limb motor function and ability in activities of daily living. NeuroRehab. 2014;35:381–389.
   PubMed Web of Science ®Google Scholar
• Ke Z, Yip YP, Li L, et al. The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: A rat brain ischemia model. PLoS One. 2011;6(2): e16643. doi: 10.1371/journal.pone.0016643.
   PubMed Web of Science ®Google Scholar
• Xiang Y, Liu H, Yan T, et al. Functional electrical stimulation-facilitated proliferation and regeneration of neural precursor cells in the brains of rats with cerebral infarction. Neural Regen Res. 2014;9:243–251.
   PubMed Web of Science ®Google Scholar
• Liu H, Xiang Y, Yan T, et al. Functional electrical stimulation increases neural stem/progenitor cell proliferation and neurogenesis in the subventricular zone of rats with stroke. Chin Med J (Engl). 2013;126:2361–2367.
   PubMed Web of Science ®Google Scholar
• Yang Y, Kimura-Ohba S, Thompson J, et al. Rodent models of vascular cognitive impairment. Transl Stroke Res. 2016;7:407–414.10.1007/s12975-016-0486-2
   PubMed Web of Science ®Google Scholar
• Murphy MP, Corriveau RA, Wilcock DM. Vascular contributions to cognitive impairment and dementia (VCID). Biochim Biophys Acta. 2016;1862:857–859.10.1016/j.bbadis.2016.02.010
   PubMed Web of Science ®Google Scholar
• Farkas E, Luiten PG, Bari F. Permanent, bilateral common carotid artery occlusion in the rat: A model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev. 2007;54:162–180.10.1016/j.brainresrev.2007.01.003
   PubMedGoogle Scholar
• Sinclair L, Tayler H, Love S. Synaptic protein levels altered in vascular dementia. Neuropathol Appl Neurobiol. 2015;41:533–543.10.1111/nan.12215
   PubMed Web of Science ®Google Scholar
• Song SH, Augustine GJ. Synapsin isoforms and synaptic vesicle trafficking. Mol Cells. 2015;38:936–940.
   PubMed Web of Science ®Google Scholar
• Wang H, Peng RY. Basic roles of key molecules connected with NMDAR signaling pathway on regulating learning and memory and synaptic plasticity. Mil Med Res. doi: 10.1186/s40779-016-0095-0.
   Google Scholar
• Yan WH, Cao MD, Liu JR. Effects of EGF and bFGF on expression of microtubule-associated protein tau and MAP-2 mRNA in human umbilical cord mononuclear cells. Cell Biol Int. 2005;29:153–157.10.1016/j.cellbi.2004.10.001
   PubMed Web of Science ®Google Scholar
• Cottrell JR, Dubé GR, Egles C, et al. Distribution, density, and clustering of functional glutamate receptors before and after synaptogenesis in hippocampal neurons. J Neurophysiol. 2000;84:1573–1587.
   PubMed Web of Science ®Google Scholar
• Isaac JT, Nicoll RA, Malenka RC. Evidence for silent synapses: Implications for the expression of LTP. Neuron. 1995;15:427–434.10.1016/0896-6273(95)90046-2
   PubMed Web of Science ®Google Scholar
• Collingridge GL, Isaac JT, Wang YT. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci. 2004;5:952–962.10.1038/nrn1556
   PubMed Web of Science ®Google Scholar
• Wang WS, Kang S, Liu WT, et al. Extinction of aversive memories associated with morphine withdrawal requires ERK-mediated epigenetic regulation of brain-derived neurotrophic factor transcription in the rat ventromedial prefrontal cortex. J Neurosci. 2012;32:13763–13775.10.1523/JNEUROSCI.1991-12.2012
   PubMed Web of Science ®Google Scholar
• Hannesson DK, Howland JG, Phillips AG. Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats. J Neurosci. 2004;24:4596–4604.10.1523/JNEUROSCI.5517-03.2004
   PubMed Web of Science ®Google Scholar
• Meunier M, Bachevalier J, Mishkin M. Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychologia. 1997;35:999–1015.10.1016/S0028-3932(97)00027-4
   PubMed Web of Science ®Google Scholar
• Zhou LY, Wright TE, Clarkson AN. Prefrontal cortex stroke induces delayed impairment in spatial memory. Behav Brain Res. 2016;296:373–378.10.1016/j.bbr.2015.08.022
   PubMed Web of Science ®Google Scholar
• Garnier C, Falempin M, Canu MH. A 3D analysis of foreand hindlimb motion during locomotion: Comparison of overground and ladder walking in rats. Behav Brain Res. 2008;186:57–65.10.1016/j.bbr.2007.07.023
   PubMed Web of Science ®Google Scholar
• Barker GR, Bird F, Alexander V, et al. Recognition memory for objects, place, and temporal order: A disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci. 2007;27:2948–2957.10.1523/JNEUROSCI.5289-06.2007
   PubMed Web of Science ®Google Scholar
• Ennaceur A, Neave N, Aggleton JP. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res. 1997;113:509–519.10.1007/PL00005603
   PubMed Web of Science ®Google Scholar
• Bevins RA, Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study ‘recognition memory’. Nat Protoc. 2006;1:1306–1311.10.1038/nprot.2006.205
   PubMed Web of Science ®Google Scholar
• Bertaina-Anglade V, Enjuanes E, Morillon D, et al. The object recognition task in rats and mice: A simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity. J Pharmacol Toxicol Methods. 2006;54:99–105.10.1016/j.vascn.2006.04.001
   PubMedGoogle Scholar
• Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 7th ed. Amsterdam: Elsevier; 2014.
   Google Scholar
• Zhou LY, Wright TE, Clarkson AN. Prefrontal cortex stroke induces delayed impairment in spatial memory. Behav Brain Res. 2016;296:373–378.10.1016/j.bbr.2015.08.022
   PubMed Web of Science ®Google Scholar
• Bachevalier J, Nemanic S. Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus. 2008;18:64–80.10.1002/(ISSN)1098-1063
   PubMed Web of Science ®Google Scholar
• Leasure JL, Jones M. Forced and voluntary exercise differentially affect brain and behavior. Neuroscience. 2008;156:456–465.10.1016/j.neuroscience.2008.07.041
   PubMed Web of Science ®Google Scholar
• Greenwood BN, Loughridge AB, Sadaoui N, et al. The protective effects of voluntary exercise against the behavioral consequences of uncontrollable stress persist despite an increase in anxiety following forced cessation of exercise. Behav Brain Res. 2012;233:314–321.10.1016/j.bbr.2012.05.017
   PubMed Web of Science ®Google Scholar
• Yuede CM, Zimmerman SD, Dong H, et al. Effects of voluntary and forced exercise on plaque deposition, hippocampal volume, and behavior in the Tg2576 mouse model of Alzheimer’s disease. Neurobiol Dis. 2009;35:426–432.10.1016/j.nbd.2009.06.002
   PubMed Web of Science ®Google Scholar
• Arida RM, Scorza CA, da Silva AV, et al. Differential effects of spontaneous versus forced exercise in rats on the staining of parvalbumin-positive neurons in the hippocampal formation. Neurosci Lett. 2004;364:135–138.10.1016/j.neulet.2004.03.086
   PubMed Web of Science ®Google Scholar
• Tiozzo E, Youbi M, Dave K, et al. Aerobic, resistance and cognitive exercise training poststroke. Stroke. 2015;46:2012–2016.10.1161/STROKEAHA.114.006649
   PubMed Web of Science ®Google Scholar
• Hara Y. Brain plasticity and rehabilitation in stroke patients. J Nippon Med Sch. 2015;82:4–13.10.1272/jnms.82.4
   PubMed Web of Science ®Google Scholar
• Caleo M. Rehabilitation and plasticity following stroke: Insights from rodent models. Neuroscience. 2015;311:180–194.10.1016/j.neuroscience.2015.10.029
   PubMed Web of Science ®Google Scholar
• Lohmann C, Kessels HW. The developmental stages of synaptic plasticity. J Physiol. 2014;592:13–31.10.1113/jphysiol.2012.235119
   PubMed Web of Science ®Google Scholar
• Brown CE, Wong C, Murphy TH. Rapid morphologic plasticity of peri-infarct dendritic spines after focal ischemic stroke. Stroke. 2008;39:1286–1291.10.1161/STROKEAHA.107.498238
   PubMed Web of Science ®Google Scholar
• Berchicci M, Lucci G, Di Russo F. Benefits of physical exercise on the aging brain: The role of the prefrontal cortex. J Gerontol A Biol Sci Med Sci. 2013;68:1337–1341.10.1093/gerona/glt094
   PubMed Web of Science ®Google Scholar
• Basso JC, Shang A, Elman M, et al. Acute exercise improves prefrontal cortex but not hippocampal function in healthy adults. J Int Neuropsychol Soc. 2015;21:791–801.10.1017/S135561771500106X
   PubMed Web of Science ®Google Scholar
• Rosenberg T, Gal-Ben-Ari S, Dieterich DC, et al. The roles of protein expression in synaptic plasticity and memory consolidation. Front Mol Neurosci. 2014;7:86. doi: 10.3389/fnmol.2014.00086.
   PubMed Web of Science ®Google Scholar
• Melloni RH Jr, Hemmendinger LM, Hamos JE, et al. Synapsin I gene expression in the adult rat brain with comparative analysis of mRNA and protein in the hippocampus. J Comp Neurol. 1993;327:507–520.10.1002/(ISSN)1096-9861
   PubMed Web of Science ®Google Scholar
• Pagnussat AS, Simao F, Anastacio JR, et al. Effects of skilled and unskilled training on functional recovery and brain plasticity after focal ischemia in adult rats. Brain Res. 2012;1486:53–61.10.1016/j.brainres.2012.09.019
   PubMed Web of Science ®Google Scholar
• Greengard P, Valtorta F, Czernik AJ, et al. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 1993;259:780–785.10.1126/science.8430330
   PubMed Web of Science ®Google Scholar
• Ferreira AF, Real CC, Rodrigues AC, et al. Moderate exercise changes synaptic and cytoskeletal proteins in motor regions of the rat brain. Brain Res. 2010;1361:31–42.10.1016/j.brainres.2010.09.045
   PubMed Web of Science ®Google Scholar
• Cassilhas RC, Lee KS, Fernandes J, et al. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience. 2012;202:309–317.10.1016/j.neuroscience.2011.11.029
   PubMed Web of Science ®Google Scholar
• Ferreira AF, Real CC, Rodrigues AC, et al. Short-term, moderate exercise is capable of inducing structural, bdnf-independent hippocampal plasticity. Brain Res. 2011;1425:111–122.10.1016/j.brainres.2011.10.004
   PubMed Web of Science ®Google Scholar
• Hescham S, Grace L, Kellaway LA, et al. Effect of exercise on synaptophysin and calcium/calmodulin-dependent protein kinase levels in prefrontal cortex and hippocampus of a rat model of developmental stress. Metab Brain Dis. 2009;24:701–709.10.1007/s11011-009-9165-2
   PubMed Web of Science ®Google Scholar
• Gori M, Luddi A, Belmonte G, et al. Expression of microtubule associated protein 2 and synaptophysin in endometrium: high levels in deep infiltrating endometriosis lesions. Fertil Steril. 2016;105:435–443.10.1016/j.fertnstert.2015.10.024
   PubMed Web of Science ®Google Scholar
• Arendt T, Bullmann T. Neuronal plasticity in hibernation and the proposed role of the microtubule-associated protein tau as a ‘master switch’ regulating synaptic gain in neuronal networks. Am J Physiol Regul Integr Comp Physiol. 2013;305:R478–R489.10.1152/ajpregu.00117.2013
   PubMed Web of Science ®Google Scholar
• Brigman JL, Wright T, Talani G, et al. Loss of GluN2B-containing NMDA receptors in CA1 hippocampus and cortex impairs long-term depression, reduces dendritic spine density, and disrupts learning. J Neurosci. 2010;30:4590–4600.10.1523/JNEUROSCI.0640-10.2010
   PubMed Web of Science ®Google Scholar
• Wang H, Peng RY. Basic roles of key molecules connected with NMDAR signaling pathway on regulating learning and memory and synaptic plasticity. Mil Med Res. 2016;3(1):26. doi: 10.1186/s40779-016-0095-0.
   PubMed Web of Science ®Google Scholar
• Lee HK, Kirkwood A. AMPA receptor regulation during synaptic plasticity in hippocampus and neocortex. Semin Cell Dev Biol. 2011;22:514–520.10.1016/j.semcdb.2011.06.007
   PubMed Web of Science ®Google Scholar
• Shonesy BC, Jalan-Sakrikar N, Cavener VS, et al. CaMKII: a molecular substrate for synaptic plasticity and memory. Prog Mol Biol Transl Sci. 2014;122:61–87.10.1016/B978-0-12-420170-5.00003-9
   PubMed Web of Science ®Google Scholar
• Yabuki Y, Nakagawasai O, Moriguchi S, et al. Decreased CaMKII and PKC activities in specific brain regions are associated with cognitive impairment in neonatal ventral hippocampus-lesioned rats. Neuroscience. 2013;234:103–115.10.1016/j.neuroscience.2012.12.048
   PubMed Web of Science ®Google Scholar
• Xu B, Yan T, Yang Y, et al. Effect of normal-walking-pattern-based functional electrical stimulation on gait of the lower extremity in subjects with ischemic stroke: A self controlled study. NeuroRehab. 2016;38:163–169.10.3233/NRE-161306
   PubMed Web of Science ®Google Scholar