Remote limb ischemic conditioning enhances motor learning in healthy humans

Journal of Neurophysiology

Volumn 113, Issue 10, 2015, Pages 3708-3719

  Cherry Allen, Kendra M ^a   Gidday, Jeff M ^a   Lee, Jin Moo ^a   Hershey, Tamara ^a   Lang, Catherine E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Behavioral training; Motor learning; Remote limb ischemic conditioning

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

ADULT; ARTICLE; CARDIOVASCULAR EFFECT; CARDIOVASCULAR FUNCTION; COGNITION; COMORBIDITY; CONTROLLED STUDY; FEMALE; FLEXOR MUSCLE; GRIP STRENGTH; HUMAN; HUMAN EXPERIMENT; LIMB ISCHEMIA; MALE; MOTOR PERFORMANCE; MUSCLE STRENGTH; NERVE CELL PLASTICITY; NORMAL HUMAN; OXYGEN SATURATION; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL; RECOGNITION; REMOTE LIMB ISCHEMIC CONDITIONING; RESPONSE TIME; SOMATOSENSORY SYSTEM; SYSTOLIC BLOOD PRESSURE; ADOLESCENT; ELECTROMYOGRAPHY; FOLLOW UP; ISCHEMIA; LEARNING; LIMB; LONG TERM MEMORY; MOVEMENT (PHYSIOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; REACTION TIME; VASCULARIZATION; YOUNG ADULT;

ADOLESCENT; ADULT; ELECTROMYOGRAPHY; EXTREMITIES; FOLLOW-UP STUDIES; HUMANS; ISCHEMIA; LEARNING; MALE; MOVEMENT; MUSCLE STRENGTH; REACTION TIME; RETENTION (PSYCHOLOGY); YOUNG ADULT;

EID: 84930839973     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01028.2014     Document Type: Article

References (122)

1. Ali ZA, Callaghan CJ, Lim E, Ali AA, Nouraei SA, Akthar AM, Boyle JR, Varty K, Kharbanda RK, Dutka DP, Gaunt ME. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation 116: 98–105, 2007.
2. Baker TL, Mitchell GS. Episodic but not continuous hypoxia elicits longterm facilitation of phrenic motor output in rats. J Physiol 529: 215–219, 2000.
3. Baker-Herman TL, Fuller DD, Bavis RW, Zabka AG, Golder FJ, Doperalski NJ, Johnson RA, Watters JJ, Mitchell GS. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat Neurosci 7: 48–55, 2004.
4. Baker-Herman TL, Mitchell GS. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22: 6239–6246, 2002.
5. Balota DA, Yap MJ, Cortese MJ, Hutchison KA, Kessler B, Loftis B, Neely JH, Nelson DL, Simpson GB, Treiman R. The English Lexicon Project. Behav Res Methods 39: 445–459, 2007.
6. Bilgin-Freiert A, Dusick JR, Stein NR, Etchepare M, Vespa P, Gonzalez NR. Muscle microdialysis to confirm sublethal ischemia in the induction of remote ischemic preconditioning. Transl Stroke Res 3: 266–272, 2012.
7. Birnbaum Y, Hale SL, Kloner RA. Ischemic preconditioning at a distance: reduction of myocardial infarct size by partial reduction of blood supplycombined with rapid stimulation of the gastrocnemius muscle in the rabbit. Circulation 96: 1641–1646, 1997.
8. Botker HE, Kharbanda R, Schmidt MR, Bottcher M, Kaltoft AK, Terkelsen CJ, Munk K, Andersen NH, Hansen TM, Trautner S, Lassen JF, Christiansen EH, Krusell LR, Kristensen SD, Thuesen L, Nielsen SS, Rehling M, Sorensen HT, Redington AN, Nielsen TT. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet 375: 727–734, 2010.
9. Brand D, Ratan RR. Epigenetics and the environment: in search of the “toleroasome” vital to execution of ischemic preconditioning. Transl Stroke Res 4: 56–62, 2013.
10. Brasil-Neto JP, Valls-Sole J, Pascual-Leone A, Cammarota A, Amassian VE, Cracco R, Maccabee P, Cracco J, Hallett M, Cohen LG. Rapid modulation of human cortical motor outputs following ischaemic nerve block. Brain 116: 511–525, 1993.
11. Brevoord D, Kranke P, Kuijpers M, Weber N, Hollmann M, Preckel B. Remote ischemic conditioning to protect against ischemia-reperfusion injury: a systematic review and meta-analysis. PLoS One 7: e42179, 2012.
12. Brooks MJ, Andrews DT. Molecular mechanisms of ischemic conditioning: translation into patient outcomes. Future Cardiol 9: 549–568, 2013.
13. Bunge SA, Burrows B, Wagner AD. Prefrontal and hippocampal contributions to visual associative recognition: interactions between cognitive control and episodic retrieval. Brain Cogn 56: 141–152, 2004.
14. Cherry KM, Lenze EJ, Lang CE. Combining D-cycloserine with motor training does not result in improved general motor learning in neurologically intact people or in people with stroke. J Neurophysiol 111: 2516–2524, 2014.
15. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 47: 2277–2282, 2006.
16. Cirelli C, Faraguna U, Tononi G. Changes in brain gene expression after long-term sleep deprivation. J Neurochem 98: 1632–1645, 2006.
17. Conner JM, Lauterborn JC, Yan Q, Gall CM, Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J Neurosci 17: 2295–2313, 1997.
18. Connolly M, Bilgin-Freiert A, Ellingson B, Dusick JR, Liebeskind D, Saver J, Gonzalez NR. Peripheral vascular disease as remote ischemic preconditioning, for acute stroke. Clin Neurol Neurosurg 115: 2124–2129, 2013.
19. Corbett D, Nguemeni C, Gomez-Smith M. How can you mend a broken brain? Neurorestorative approaches to stroke recovery. Cerebrovasc Dis 38: 233–239, 2014.
20. Cramer SC, Sur M, Dobkin BH, O’Brien C, Sanger TD, Trojanowski JQ, Rumsey JM, Hicks R, Cameron J, Chen D, Chen WG, Cohen LG, deCharms C, Duffy CJ, Eden GF, Fetz EE, Filart R, Freund M, Grant SJ, Haber S, Kalivas PW, Kolb B, Kramer AF, Lynch M, Mayberg HS, McQuillen PS, Nitkin R, Pascual-Leone A, Reuter-Lorenz P, Schiff N, Sharma A, Shekim L, Stryker M, Sullivan EV, Vinogradov S. Harnessing neuroplasticity for clinical applications. Brain 134: 1591–1609, 2011.
21. Cubeddu A, Bucci F, Giannini A, Russo M, Daino D, Russo N, Merlini S, Pluchino N, Valentino V, Casarosa E, Luisi S, Genazzani AR. Brainderived neurotrophic factor plasma variation during the different phases of the menstrual cycle in women with premenstrual syndrome. Psychoneuroendocrinology 36: 523–530, 2011.
22. Cunha C, Brambilla R, Thomas KL. A simple role for BDNF in learning and memory? Front Mol Neurosci 3: 1, 2010.
23. Dale-Nagle EA, Hoffman MS, MacFarlane PM, Satriotomo I, Lovett-Barr MR, Vinit S, Mitchell GS. Spinal plasticity following intermittent hypoxia: implications for spinal injury. Ann NY Acad Sci 1198: 252–259, 2010.
24. Dickson EW, Reinhardt CP, Renzi FP, Becker RC, Porcaro WA, Heard SO. Ischemic preconditioning may be transferable via whole blood transfusion: preliminary evidence. J Thromb Thrombolysis 8: 123–129, 1999.
25. Ding Q, Ying Z, Gomez-Pinilla F. Exercise influences hippocampal plasticity by modulating brain-derived neurotrophic factor processing. Neuroscience 192: 773–780, 2011.
26. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8: 398–412, 2009.
27. Drager LF, Jun JC, Polotsky VY. Metabolic consequences of intermittent hypoxia: relevance to obstructive sleep apnea. Best Pract Res Clin Endocrinol Metab 24: 843–851, 2010.
28. Duzel E, Habib R, Rotte M, Guderian S, Tulving E, Heinze HJ. Human hippocampal and parahippocampal activity during visual associative recognition memory for spatial and nonspatial stimulus configurations. J Neurosci 23: 9439–9444, 2003.
29. Edelmann E, Lessmann V, Brigadski T. Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity. Neuropharmacology 76C: 610–627, 2014.
30. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 112: 257–269, 2003.
31. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 96: 1486–1495, 2004.
32. Ferris LT, Williams JS, Shen CL. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc 39: 728–734, 2007.
33. Flor H, Braun C, Elbert T, Birbaumer N. Extensive reorganization of primary somatosensory cortex in chronic back pain patients. Neurosci Lett 224: 5–8, 1997.
34. Fuller DD, Johnson SM, Olson EB, Mitchell GS. Synaptic pathways to phrenic motoneurons are enhanced by chronic intermittent hypoxia after cervical spinal cord injury. J Neurosci 23: 2993–3000, 2003.
35. Gho BC, Schoemaker RG, van den Doel MA, Duncker DJ, Verdouw PD. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 94: 2193–2200, 1996.
36. Gidday JM. Cerebral preconditioning and ischaemic tolerance. Nat Rev Neurosci 7: 437–448, 2006.
37. Giehl KM, Schutte A, Mestres P, Yan Q. The survival-promoting effect of glial cell line-derived neurotrophic factor on axotomized corticospinal neurons in vivo is mediated by an endogenous brain-derived neurotrophic factor mechanism. J Neurosci 18: 7351–7360, 1998.
38. Golder FJ, Mitchell GS. Spinal synaptic enhancement with acute intermittent hypoxia improves respiratory function after chronic cervical spinal cord injury. J Neurosci 25: 2925–2932, 2005.
39. Gonzalez NR, Connolly M, Dusick JR, Bhakta H, Vespa P. Phase I clinical trial for the feasibility and safety of remote ischemic conditioning for aneurysmal subarachnoid hemorrhage. Neurosurgery 75: 590–598, 2014.
40. Hairston IS, Peyron C, Denning DP, Ruby NF, Flores J, Sapolsky RM, Heller HC, O’Hara BF. Sleep deprivation effects on growth factor expression in neonatal rats: a potential role for BDNF in the mediation of delta power. J Neurophysiol 91: 1586–1595, 2004.
41. Hall J, Thomas KL, Everitt BJ. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3: 533–535, 2000.
42. Hamilton A, Balnave R, Adams R. Grip strength testing reliability. J Hand Ther 7: 163–170, 1994.
43. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research Electronic Data Capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42: 377–381, 2009.
44. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, Hayward M, Keogh B, MacAllister RJ, Yellon DM. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370: 575–579, 2007.
45. Hausenloy DJ, Yellon DM. Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res 79: 377–386, 2008.
46. Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis 204: 334–341, 2009.
47. Hausenloy DJ, Yellon DM. The therapeutic potential of ischemic conditioning: an update. Nat Rev Cardiol 8: 619–629, 2011.
48. Hayes HB, Jayaraman A, Herrmann M, Mitchell GS, Rymer WZ, Trumbower RD. Daily intermittent hypoxia enhances walking after chronic spinal cord injury: a randomized trial. Neurology 82: 104–113, 2014.
49. Hess DC, Hoda MN, Bhatia K. Remote limb perconditioning [corrected] and postconditioning: will it translate into a promising treatment for acute stroke? Stroke 44: 1191–1197, 2013.
50. Hougaard KD, Hjort N, Zeidler D, Sorensen L, Norgaard A, Hansen TM, von Weitzel-Mudersbach P, Simonsen CZ, Damgaard D, Gottrup H, Svendsen K, Rasmussen PV, Ribe LR, Mikkelsen IK, Nagenthiraja K, Cho TH, Redington AN, Botker HE, Ostergaard L, Mouridsen K, Andersen G. Remote ischemic perconditioning as an adjunct therapy to thrombolysis in patients with acute ischemic stroke: a randomized trial. Stroke 45: 159–167, 2014.
51. Iadecola C, Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat Neurosci 14: 1363–1368, 2011.
52. Ishida T, Yarimizu K, Gute DC, Korthuis RJ. Mechanisms of ischemic preconditioning. Shock 8: 86–94, 1997.
53. Janda DH, Geiringer SR, Hankin FM, Barry DT. Objective evaluation of grip strength. J Occup Environ Med 29: 569–571, 1987.
54. Jennings RB, Murry CE, Reimer KA. Preconditioning myocardium with ischemia. Cardiovasc Drugs Ther 5: 933–938, 1991.
55. Jickling GC, Sharp FR. Blood biomarkers of ischemic stroke. Neurotherapeutics 8: 349–360, 2011.
56. Katoh-Semba R, Wakako R, Komori T, Shigemi H, Miyazaki N, Ito H, Kumagai T, Tsuzuki M, Shigemi K, Yoshida F, Nakayama A. Agerelated changes in BDNF protein levels in human serum: differences between autism cases and normal controls. Int J Dev Neurosci 25: 367–372, 2007.
57. Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 106: 2881–2883, 2002.
58. Kharbanda RK, Nielsen TT, Redington AN. Translation of remote ischaemic preconditioning into clinical practice. Lancet 374: 1557–1565, 2009.
59. Kleim JA, Chan S, Pringle E, Schallert K, Procaccio V, Jimenez R, Cramer SC. BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9: 735–737, 2006.
60. Koch S. Preconditioning the human brain: practical considerations for proving cerebral protection. Transl Stroke Res 1: 161–169, 2010.
61. Koch S. Moving towards preconditioning for neurological disorders: are we ready for clinical trials? Transl Stroke Res 4: 15–18, 2013.
62. Koch S, Della-Morte D, Dave KR, Sacco RL, Perez-Pinzon MA. Biomarkers for ischemic preconditioning: finding the responders. J Cereb Blood Flow Metab 34: 933–941, 2014.
63. Koch S, Gonzalez N. Preconditioning the human brain: proving the principle in subarachnoid hemorrhage. Stroke 44: 1748–1753, 2013.
64. Koch S, Katsnelson M, Dong C, Perez-Pinzon M. Remote ischemic limb preconditioning after subarachnoid hemorrhage: a phase Ib study of safety and feasibility. Stroke 42: 1387–1391, 2011.
65. Konstantinov IE, Li J, Cheung MM, Shimizu M, Stokoe J, Kharbanda RK, Redington AN. Remote ischemic preconditioning of the recipient reduces myocardial ischemia-reperfusion injury of the denervated donor heart via a KATP channel-dependent mechanism. Transplantation 79: 1691–1695, 2005.
66. Krakauer JW, Carmichael ST, Corbett D, Wittenberg GF. Getting neurorehabilitation right: what can be learned from animal models? Neurorehabil Neural Repair 26: 923–931, 2012.
67. Kuzuya T, Hoshida S, Yamashita N, Fuji H, Oe H, Hori M, Kamada T, Tada M. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia. Circ Res 72: 1293–1299, 1993.
68. Laskey WK. Brief repetitive balloon occlusions enhance reperfusion during percutaneous coronary intervention for acute myocardial infarction: a pilot study. Catheter Cardiovasc Interv 65: 361–367, 2005.
69. Levy LM, Ziemann U, Chen R, Cohen LG. Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation. Ann Neurol 52: 755–761, 2002.
70. Lim SY, Yellon DM, Hausenloy DJ. The neural and humoral pathways in remote limb ischemic preconditioning. Basic Res Cardiol 105: 651–655, 2010.
71. Ling L, Fuller DD, Bach KB, Kinkead R, Olson EB, Mitchell GS. Chronic intermittent hypoxia elicits serotonin-dependent plasticity in the central neural control of breathing. J Neurosci 21: 5381–5388, 2001.
72. Liu XQ, Sheng R, Qin ZH. The neuroprotective mechanism of brain ischemic preconditioning. Acta Pharmacol Sin 30: 1071–1080, 2009.
73. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, Virchow JC. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging 26: 115–123, 2005.
74. Lovett-Barr MR, Satriotomo I, Muir GD, Wilkerson JE, Hoffman MS, Vinit S, Mitchell GS. Repetitive intermittent hypoxia induces respiratory and somatic motor recovery after chronic cervical spinal injury. J Neurosci 32: 3591–3600, 2012.
75. Mathiowetz V, Weber K, Volland G, Kashman N. Reliability and validity of grip and pinch strength evaluations. J Hand Surg 9: 222–226, 1984.
76. McClanahan TB, Nao BS, Wolke LJ, Martin BJ, Mertz TE, Gallagher KP. Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits (Abstract). FASEB J 7: A118, 1993.
77. McNevin NH, Shea CH, Wulf G. Increasing the distance of an external focus of attention enhances learning. Psychol Res 67: 22–29, 2003.
78. McNulty PA, Macefield VG, Taylor JL, Hallett M. Cortically evoked neural volleys to the human hand are increased during ischaemic block of the forearm. J Physiol 538: 279–288, 2002.
79. Meng R, Asmaro K, Meng L, Liu Y, Ma C, Xi C, Li G, Ren C, Luo Y, Ling F, Jia J, Hua Y, Wang X, Ding Y, Lo EH, Ji X. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79: 1853–1861, 2012.
80. Milot MH, Cramer SC. Biomarkers of recovery after stroke. Curr Opin Neurol 21: 654–659, 2008.
81. Mitchell GS, Baker TL, Nanda SA, Fuller DD, Zabka AG, Hodgeman BA, Bavis RW, Mack KJ, Olson EB. Intermittent hypoxia and respiratory plasticity. J Appl Physiol (1985) 90: 2466–2475, 2001.
82. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124–1136, 1986.
83. Oxman T, Arad M, Klein R, Avazov N, Rabinowitz B. Limb ischemia preconditions the heart against reperfusion tachyarrhythmia. Am J Physiol Heart Circ Physiol 273: H1707–H1712, 1997.
84. Patel HH, Moore J, Hsu AK, Gross GJ. Cardioprotection at a distance: mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism. J Mol Cell Cardiol 34: 1317–1323, 2002.
85. Pearson-Fuhrhop KM, Kleim JA, Cramer SC. Brain plasticity and genetic factors. Top Stroke Rehabil 16: 282–299, 2009.
86. Pell TJ, Baxter GF, Yellon DM, Drew GM. Renal ischemia preconditions myocardium: role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol Heart Circ Physiol 275: H1542–H1547, 1998.
87. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. Regional ischemic “preconditioning” protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 87: 893–899, 1993.
88. Reaz M, Hussain M, Mohd-Yasin F. Techniques of EMG signal analysis: detection, processing, classification and applications. Biol Proced Online 8: 11–35, 2006.
89. Ren C, Gao X, Steinberg GK, Zhao H. Limb remote-preconditioning protects against focal ischemia in rats and contradicts the dogma of therapeutic time windows for preconditioning. Neuroscience 151: 1099–1103, 2008.
90. Satriotomo I, Dale EA, Dahlberg JM, Mitchell GS. Repetitive acute intermittent hypoxia increases expression of proteins associated with plasticity in the phrenic motor nucleus. Exp Neurol 237: 103–115, 2012.
91. Saxena P, Newman MA, Shehatha JS, Redington AN, Konstantinov IE. Remote ischemic conditioning: evolution of the concept, mechanisms, and clinical application. J Card Surg 25: 127–134, 2010.
92. Schaefer SY, Lang CE. Using dual tasks to test immediate transfer of training between naturalistic movements: a proof-of-principle study. J Mot Behav 44: 313–327, 2012.
93. Schinder AF, Poo M. The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23: 639–645, 2000.
94. Shimizu M, Tropak M, Diaz RJ, Suto F, Surendra H, Kuzmin E, Li J, Gross G, Wilson GJ, Callahan J, Redington AN. Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci 117: 191–200, 2009.
95. Siddall PJ. Neuroplasticity and pain: what does it all mean? Med J Aust 198: 177–178, 2013.
96. Snodgrass JG, Corwin J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol Gen 117: 34–50, 1988.
97. Staat P, Rioufol G, Piot C, Cottin Y, Cung TT, L’Huillier I, Aupetit JF, Bonnefoy E, Finet G, Andre-Fouet X, Ovize M. Postconditioning the human heart. Circulation 112: 2143–2148, 2005.
98. Stapels M, Piper C, Yang T, Li M, Stowell C, Xiong ZG, Saugstad J, Simon RP, Geromanos S, Langridge J, Lan JQ, Zhou A. Polycomb group proteins as epigenetic mediators of neuroprotection in ischemic tolerance. Sci Signal 3: 111, 2010.
99. Stetler RA, Leak RK, Gan Y, Li P, Zhang F, Hu X, Jing Z, Chen J, Zigmond MJ, Gao Y. Preconditioning provides neuroprotection in modelsof CNS disease: paradigms and clinical significance. Prog Neurobiol 114: 58–83, 2014.
100. Stowell C, Wang L, Arbogast B, Lan JQ, Cioffi GA, Burgoyne CF, Zhou A. Retinal proteomic changes under different ischemic conditions—implication of an epigenetic regulatory mechanism. Int J Physiol Pathophysiol Pharmacol 2: 148–160, 2010.
101. Tang SW, Chu E, Hui T, Helmeste D, Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci Lett 431: 62–65, 2008.
102. Tapuria N, Kumar Y, Habib MM, Abu Amara M, Seifalian AM, Davidson BR. Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury—a review. J Surg Res 150: 304–330, 2008.
103. Taubert M, Draganski B, Anwander A, Muller K, Horstmann A, Villringer A, Ragert P. Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J Neurosci 30: 11670–11677, 2010.
104. Thoenen H. Neurotrophins and neuronal plasticity. Science 270: 593–598, 1995.
105. Thoenen H. Neurotrophins and activity-dependent plasticity. Prog Brain Res 128: 183–191, 2000.
106. Thompson JW, Narayanan SV, Koronowski KB, Morris-Blanco K, Dave KR, Perez-Pinzon MA. Signaling pathways leading to ischemic mitochondrial neuroprotection. J Bioenerg Biomembr 47: 101–110, 2015.
107. Toraman A, Yildirim NU. The falling risk and physical fitness in older people. Arch Gerontol Geriatr 51: 222–226, 2010.
108. Trumbower RD, Jayaraman A, Mitchell GS, Rymer WZ. Exposure to acute intermittent hypoxia augments somatic motor function in humans with incomplete spinal cord injury. Neurorehabil Neural Repair 26: 163–172, 2012.
109. Turner DL, Mitchell GS. Long-term facilitation of ventilation following repeated hypoxic episodes in awake goats. J Physiol 499: 543–550, 1997.
110. Vinten-Johansen J, Shi W. The science and clinical translation of remote postconditioning. J Cardiovasc Med (Hagerstown) 14: 206–213, 2013.
111. Werhahn KJ, Mortensen J, Kaelin-Lang A, Boroojerdi B, Cohen LG. Cortical excitability changes induced by deafferentation of the contralateral hemisphere. Brain 125: 1402–1413, 2002.
112. Wilkerson JE, Mitchell GS. Daily intermittent hypoxia augments spinal BDNF levels, ERK phosphorylation and respiratory long-term facilitation. Exp Neurol 217: 116–123, 2009.
113. Wolf DH, Gerraty R, Satterthwaite TD, Loughead J, Campellone T, Elliott MA, Turetsky BI, Gur RC, Gur RE. Striatal intrinsic reinforcement signals during recognition memory: relationship to response bias and dysregulation in schizophrenia. Front Behav Neurosci 5: 81, 2011.
114. Wulf G, Weigelt M, Poulter D, McNevin N. Attentional focus on suprapostural tasks affects balance learning. Q J Exp Psychol A 56: 1191–1211, 2003.
115. Yang Q, Wang Y, Feng J, Cao J, Chen B. Intermittent hypoxia from obstructive sleep apnea may cause neuronal impairment and dysfunction in central nervous system: the potential roles played by microglia. Neuropsychiatr Dis Treat 9: 1077–1086, 2013.
116. Yarrow JF, White LJ, McCoy SC, Borst SE. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett 479: 161–165, 2010.
117. Yonelinas AP, Hopfinger JB, Buonocore MH, Kroll NE, Baynes K. Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study. Neuroreport 12: 359–363, 2001.
118. Zhao H. Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29: 873–885, 2009.
119. Zhao H. Hurdles to clear before clinical translation of ischemic postconditioning against stroke. Transl Stroke Res 4: 63–70, 2013.
120. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285: H579–H588, 2003.
121. Ziemann U, Corwell B, Cohen LG. Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18: 1115–1123, 1998a.
122. Ziemann U, Hallett M, Cohen LG. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18: 7000–7007, 1998b.