Involuntary, forced and voluntary exercises are equally capable of inducing hippocampal plasticity and the recovery of cognitive function after stroke

Neurological Research

Volumn 37, Issue 10, 2015, Pages 893-901

  Lin, Yangyang ^a   Dong, Juntao ^a   Yan, Tiebin ^a   He, Xiaokuo ^b   Zheng, Xiuyuan ^a   Liang, Huiying ^c   Sui, Minghong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b Shiyan Taihe Hospital   (China)

^c People s Hospital of Zhongshan City   (China)

Author keywords

Cognition; Dementia; Exercise; Functional electrical stimulation; Hippocampus; Plasticity; Stroke

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 2; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPSIN I; SYNAPTOPHYSIN; TAU PROTEIN; DLGH4 PROTEIN, RAT; MAPT PROTEIN, RAT; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; SIGNAL PEPTIDE; SYNAPSIN; SYP PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROVASCULAR ACCIDENT; COGNITION; CONTROLLED STUDY; DEMENTIA; EXERCISE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL PLASTICITY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; RAT; WESTERN BLOTTING; ANIMAL; ELECTROSTIMULATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RECOGNITION; STROKE; WISTAR RAT;

ANIMALS; COGNITION; ELECTRIC STIMULATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); STROKE; SYNAPSINS; SYNAPTOPHYSIN; TAU PROTEINS;

EID: 84940189086     PISSN: 01616412     EISSN: 17431328     Source Type: Journal    
DOI: 10.1179/1743132815Y.0000000074     Document Type: Article

References (39)

1. Ammann BC, Knols RH, Baschung P, de Bie RA, de Bruin ED. Application of principles of exercise training in sub-acute and chronic stroke survivors: a systematic review. BMC Neurol. 2014;14:167
2. Tajiri N, Yasuhara T, Shingo T, Kondo A, Yuan W, Kadota T, et al. Exercise exerts neuroprotective effects on Parkinson’s disease model of rats. Brain Res. 2009;1310:200–7
3. Ploughman M, Granter-Button S, Chernenko G, Tucker BA, Mearow KM, Corbett D. Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin- I and insulin-like growth factor I after focal ischemia. Neuroscience. 2005;136:991–1001
4. Shimada H, Hamakawa M, Ishida A, Tamakoshi K, Nakashima H, Ishida K. Low-speed treadmill running exercise improves memory function after transient middle cerebral artery occlusionin rats. Behav Brain Res. 2013;243:21–7
5. Nakajima S, Ohsawa I, Ohta S, Ohno M, Mikami T. Regular voluntary exercise cures stress-induced impairment of cognitive function and cell proliferation accompanied by increases in cerebral IGF-1 and GST activity in mice. Behav Brain Res. 2010;211:178–84
6. Alomari MA, Khabour OF, Alzoubi KH, Alzubi MA. Forced and voluntary exercises equally improve spatial learning and memory and hippocampal BDNF levels. Behav Brain Res. 2013;247:34–9
7. Kishi T, Sunagawa K. Exercise training plus calorie restriction causes synergistic protection against cognitive decline via upregulation of BDNF in hippocampus of stroke-prone hypertensive rats. Conf Proc IEEE Eng Med Biol Soc. 2012;2012:6764–7
8. Stranahan AM, Khalil D, Gould E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus. 2007;17:1017–22
9. Pysh JJ, Weiss GM. Exercise during development induces an increase in Purkinje cell dendritic tree size. Science. 2007;206:230–2
10. 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:H620–33
11. Jing YE, Nakashima Y, Zhang B, Kobayashi Y, Fujie MG. Functional electrical stimulation based on a pelvis support robot for gait rehabilitation of hemiplegic patients after stroke. Conf Proc IEEE EngMed Biol Soc. 2014;2014:3098–101
12. 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;36:80–5
13. Burnett MG, Shimazu T, Szabados T, Muramatsu H, Detre JA, Greenberg JH. Electrical forepaw stimulation during reversible forebrain ischemia decreases infarct volume. Stroke. 2006;37:1327–31
14. Leung LY, Tong KY, Zhang SM, Zeng XH, Zhang KP, Zheng XX. Neurochemical effects of exercise and neuromuscular electrical stimulation on brain after stroke: a microdialysis study using rat model. Neurosci Lett. 2006;397:135–9
15. Nanri M, Watanabe H. Availability of 2VO rats as a model for chronic cerebrovascular disease. Nihon Yakurigaku Zasshi. 1999;113:85–95
16. Jellinger KA. The enigma of vascular cognitive disorder and vascular dementia. Acta Neuropathol. 2007;113:349–88
17. Wang F, Chang G, Geng X. NGF and TERT co-transfected BMSCs improve the restoration of cognitive impairment in vascular dementia rats. PLoS One. 2014;9:e98774
18. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel DW Jr, et al. Altered expression of synaptic proteins occurs early during progression of Alzheimer’s disease. Neurology. 2001;56:127–9
19. Mundy WR, Robinette B, Radio NM, Freudenrich TM. Protein biomarkers associated with growth and synaptogenesis in a cell culture model of neuronal development. Toxicology. 2008;249:220–9
20. Leuba G, Savioz A, Vernay A, Carnal B, Kraftsik R, Tardif E, et al. Differential changes in synaptic proteins in the Alzheimer frontal cortex with marked increase in PSD-95 postsynaptic protein. J Alzheimers Dis. 2008;15:139–51
21. 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;54:162–80
22. Garnier C, Falempin M, Canu MH. A 3D analysis of fore- and hindlimb motion during locomotion: comparison of overground and ladder walking in rats. Behav Brain Res. 2008;186:57–65
23. Whishaw IQ, Travis SG, Koppe SW, Sacrey LA, Gholamrezaei G, Gorny B.Hand shaping in the rat: conserved release and collection vs. flexible manipulation in overground walking, ladder rung walking, cylinder exploration, and skilled reaching. Behav Brain Res. 2010;206:21–31
24. Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats: 1: behavioral data. Behav Brain Res. 1998;31:47–59
25. 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; 113:509–19
26. Xiang Y, Liu H, Yan T, Zhuang Z, Jin D, Peng Y. Functional electrical stimulation-facilitated proliferation and regeneration of neural precursor cells in the brains of rats with cerebral infarction. Neural Regen Res. 2014;9:243–51
27. Ke Z, Yip SP, Li L, Zheng XX, Tong KY. 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:e16643
28. Fornasiero EF, Raimondi A, Guarnieri FC, Orlando M, Fesce R, Benfenati F, et al. Synapsins contribute to the dynamic spatial organization of synaptic vesicles in an activity-dependent manner. J Neurosci. 2012;32:12214–27
29. Leugers CJ, Lee G. Tau potentiates nerve growth factorinduced mitogen-activated protein kinase signaling and neurite initiation without a requirement for microtubule binding. J Biol Chem. 2010;285:19125–34
30. Schaeffer E, Alder J, Greengard P, Poo MM. Synapsin IIa accelerates functional development of neuromuscular synapses. Proc Natl Acad Sci USA. 1994;91:3882–6
31. Ehrlich I, Klein M, Rumpel S, Malinow R. PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci USA. 2007;104:4176–81
32. Gómez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol. 2002;88: 2187–95
33. Vaynman SS, Ying Z, Yin D, Gomez-Pinilla F. Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res. 2006;1070:124–30
34. Revilla S, Suñol C, García-Mesa Y, Giménez-Llort L, Sanfeliu C, Cristófol R. Physical exercise improves synaptic dysfunction and recovers the loss of survival factors in 3xTg-AD mouse brain. Neuropharmacology. 2012;81:55–63
35. Gomes da Silva S, Unsain N, Mascó DH, Toscano-Silva M, de Amorim HA, Silva Araújo BH, et al. Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus. 2012;22:347–58
36. Auer RN, Jensen ML, Whishaw IQ. Neurobehavioral deficit due to ischemic brain damage limited to half of the CA1 sector of the hippocampus. J Neurosci. 1989;9:1641–7
37. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev. 1992; 99:195–231
38. van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA. 1999;96:13427–31
39. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N. MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol. 2002;158: 541–9.