The Effects of Exercise on Cognitive Recovery after Acquired Brain Injury in Animal Models: A Systematic Review

Elise Wogensen, Hana Malá, Jesper Mogensen, Elise Wogensen, Hana Malá, Jesper Mogensen

Abstract

The objective of the present paper is to review the current status of exercise as a tool to promote cognitive rehabilitation after acquired brain injury (ABI) in animal model-based research. Searches were conducted on the PubMed, Scopus, and psycINFO databases in February 2014. Search strings used were: exercise (and) animal model (or) rodent (or) rat (and) traumatic brain injury (or) cerebral ischemia (or) brain irradiation. Studies were selected if they were (1) in English, (2) used adult animals subjected to acquired brain injury, (3) used exercise as an intervention tool after inflicted injury, (4) used exercise paradigms demanding movement of all extremities, (5) had exercise intervention effects that could be distinguished from other potential intervention effects, and (6) contained at least one measure of cognitive and/or emotional function. Out of 2308 hits, 22 publications fulfilled the criteria. The studies were examined relative to cognitive effects associated with three themes: exercise type (forced or voluntary), timing of exercise (early or late), and dose-related factors (intensity, duration, etc.). The studies indicate that exercise in many cases can promote cognitive recovery after brain injury. However, the optimal parameters to ensure cognitive rehabilitation efficacy still elude us, due to considerable methodological variations between studies.

References

    1. Cordero A., Masiá M. D., Galve E. Physical Exercise and Health. Revista Española de Cardiología (English Edition) 2014;67(9):748–753. doi: 10.1016/j.rec.2014.04.005.
    1. Penedo F. J., Dahn J. R. Exercise and well-being: a review of mental and physical health benefits associated with physical activity. Current Opinion in Psychiatry. 2005;18(2):189–193. doi: 10.1097/00001504-200503000-00013.
    1. Pérez A. B. Exercise as the cornerstone of cardiovascular prevention. Revista Espanola de Cardiologia. 2008;61(5):514–528. doi: 10.1157/13119996.
    1. Cooney G., Dwan K., Mead G. Exercise for depression. JAMA. 2014;311(23):2432–2433. doi: 10.1001/jama.2014.4930.
    1. Josefsson T., Lindwall M., Archer T. Physical exercise intervention in depressive disorders: meta-analysis and systematic review. Scandinavian Journal of Medicine & Science in Sports. 2014;24(2):259–272. doi: 10.1111/sms.12050.
    1. Strickland J. C., Smith M. A. The anxiolytic effects of resistance exercise. Frontiers in Psychology. 2014;5, article 753 doi: 10.3389/fpsyg.2014.00753.
    1. Ströhle A. Physical activity, exercise, depression and anxiety disorders. Journal of Neural Transmission. 2009;116(6):777–784. doi: 10.1007/s00702-008-0092-x.
    1. Lautenschlager N. T., Almeida O. P. Physical activity and cognition in old age. Current Opinion in Psychiatry. 2006;19(2):190–193. doi: 10.1097/01.yco.0000214347.38787.37.
    1. Smith P. J., Potter G. G., McLaren M. E., Blumenthal J. A. Impact of aerobic exercise on neurobehavioral outcomes. Mental Health and Physical Activity. 2013;6(3):139–153. doi: 10.1016/j.mhpa.2013.06.008.
    1. Khan N. A., Hillman C. H. The relation of childhood physical activity and aerobic fitness to brain function and cognition: a review. Pediatric Exercise Science. 2014;26(2):138–146. doi: 10.1123/pes.2013-0125.
    1. Käll L. B., Nilsson M., Lindén T. The impact of a physical activity intervention program on academic achievement in a Swedish elementary school setting. Journal of School Health. 2014;84(8):473–480. doi: 10.1111/josh.12179.
    1. Singh A., Uijtdewilligen L., Twisk J. W. R., van Mechelen W., Chinapaw M. J. M. Physical activity and performance at school: a systematic review of the literature including a methodological quality assessment. Archives of Pediatrics & Adolescent Medicine. 2012;166(1):49–55. doi: 10.1001/archpediatrics.2011.716.
    1. Aarsland D., Sardahaee F. S., Anderssen S., Ballard C. Is physical activity a potential preventive factor for vascular dementia? A systematic review. Aging & Mental Health. 2010;14(4):386–395. doi: 10.1080/13607860903586136.
    1. McDonnell M. N., Smith A. E., MacKintosh S. F. Aerobic exercise to improve cognitive function in adults with neurological disorders: a systematic review. Archives of Physical Medicine and Rehabilitation. 2011;92(7):1044–1052. doi: 10.1016/j.apmr.2011.01.021.
    1. Rolland Y., Abellan van Kan G., Vellas B. Physical activity and Alzheimer's disease: from prevention to therapeutic perspectives. Journal of the American Medical Directors Association. 2008;9(6):390–405. doi: 10.1016/j.jamda.2008.02.007.
    1. Öhman H., Savikko N., Strandberg T. E., Pitkälä K. H. Effect of physical exercise on cognitive performance in older adults with mild cognitive impairment or dementia: a systematic review. Dementia and Geriatric Cognitive Disorders. 2014;38(5-6):347–365. doi: 10.1159/000365388.
    1. Chang H.-C., Yang Y.-R., Wang P. S., Kuo C.-H., Wang R.-Y. Insulin-like growth factor I signaling for brain recovery and exercise ability in brain ischemic rats. Medicine & Science in Sports & Exercise. 2011;43(12):2274–2280. doi: 10.1249/mss.0b013e318223b5d9.
    1. Chung J.-Y., Kim M.-W., Bang M.-S., Kim M. The effect of exercise on trkA in the contralateral hemisphere of the ischemic rat brain. Brain Research. 2010;1353:187–193. doi: 10.1016/j.brainres.2010.06.057.
    1. Chung J. Y., Kim M. W., Bang M. S., Kim M. Increased expression of neurotrophin 4 following focal cerebral ischemia in adult rat brain with treadmill exercise. PLoS ONE. 2013;8(3) doi: 10.1371/journal.pone.0052461.e52461
    1. Ke Z., Yip S. P., Li L., Zheng X.-X., Tong K.-Y. 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) doi: 10.1371/journal.pone.0016643.e16643
    1. Kim M.-W., Bang M.-S., Han T.-R., et al. Exercise increased BDNF and trkB in the contralateral hemisphere of the ischemic rat brain. Brain Research. 2005;1052(1):16–21. doi: 10.1016/j.brainres.2005.05.070.
    1. Chang H.-C., Yang Y.-R., Wang P. S., Wang R.-Y. Quercetin enhances exercise-mediated neuroprotective effects in brain ischemic rats. Medicine and Science in Sports and Exercise. 2014;46(10):1908–1916. doi: 10.1249/mss.0000000000000310.
    1. Lee M.-H., Kim H., Kim S.-S., et al. Treadmill exercise suppresses ischemia-induced increment in apoptosis and cell proliferation in hippocampal dentate gyrus of gerbils. Life Sciences. 2003;73(19):2455–2465. doi: 10.1016/s0024-3205(03)00655-6.
    1. Zhang P., Zhang Y., Zhang J., et al. Early exercise protects against cerebral ischemic injury through inhibiting neuron apoptosis in cortex in rats. International Journal of Molecular Sciences. 2013;14(3):6074–6089. doi: 10.3390/ijms14036074.
    1. Ho N. F., Han S. P., Dawe G. S. Effect of voluntary running on adult hippocampal neurogenesis in cholinergic lesioned mice. BMC Neuroscience. 2009;10, article 57 doi: 10.1186/1471-2202-10-57.
    1. Jin J., Kang H.-M., Park C. Voluntary exercise enhances survival and migration of neural progenitor cells after intracerebral haemorrhage in mice. Brain Injury. 2010;24(3):533–540. doi: 10.3109/02699051003610458.
    1. Lee H. H., Shin M. S., Kim Y. S., et al. Early treadmill exercise decreases intrastriatal hemorrhage-induced neuronal cell death and increases cell proliferation in the dentate gyrus of streptozotocin-induced hyperglycemic rats. Journal of Diabetes and its Complications. 2005;19(6):339–346. doi: 10.1016/j.jdiacomp.2005.03.006.
    1. Zhang L., Hu X., Luo J., et al. Physical exercise improves functional recovery through mitigation of autophagy, attenuation of apoptosis and enhancement of neurogenesis after MCAO in rats. BMC Neuroscience. 2013;14, article 46 doi: 10.1186/1471-2202-14-46.
    1. Matsuda F., Sakakima H., Yoshida Y. The effects of early exercise on brain damage and recovery after focal cerebral infarction in rats. Acta Physiologica. 2011;201(2):275–287. doi: 10.1111/j.1748-1716.2010.02174.x.
    1. Yang Y.-R., Wang R.-Y., Wang P. S.-G. Early and late treadmill training after focal brain ischemia in rats. Neuroscience Letters. 2003;339(2):91–94. doi: 10.1016/s0304-3940(03)00010-7.
    1. Piao C.-S., Stoica B. A., Wu J., et al. Late exercise reduces neuroinflammation and cognitive dysfunction after traumatic brain injury. Neurobiology of Disease. 2013;54:252–263. doi: 10.1016/j.nbd.2012.12.017.
    1. Lee S.-U., Kim D.-Y., Park S.-H., Choi D.-H., Park H.-W., Han T. R. Mild to moderate early exercise promotes recovery from cerebral ischemia in rats. Canadian Journal of Neurological Sciences. 2009;36(4):443–449. doi: 10.1017/s0317167100007769.
    1. Seo T.-B., Kim B.-K., Ko I.-G., et al. Effect of treadmill exercise on Purkinje cell loss and astrocytic reaction in the cerebellum after traumatic brain injury. Neuroscience Letters. 2010;481(3):178–182. doi: 10.1016/j.neulet.2010.06.087.
    1. Ma Y., Qiang L., He M. Exercise therapy augments the ischemia-induced proangiogenic state and results in sustained improvement after stroke. International Journal of Molecular Sciences. 2013;14(4):8570–8584. doi: 10.3390/ijms14048570.
    1. Zhang P., Yu H., Zhou N., et al. Early exercise improves cerebral blood flow through increased angiogenesis in experimental stroke rat model. Journal of NeuroEngineering and Rehabilitation. 2013;10(1, article 43) doi: 10.1186/1743-0003-10-43.
    1. Rabinowitz A. R., Levin H. S. Cognitive sequelae of traumatic brain injury. Psychiatric Clinics of North America. 2014;37(1):1–11. doi: 10.1016/j.psc.2013.11.004.
    1. Kleim J. A., Jones T. A. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. Journal of Speech, Language, & Hearing Research. 2008;51(1):S225–S239. doi: 10.1044/1092-4388(2008/018).
    1. Wu A., Ying Z., Gomez-Pinilla F. Exercise facilitates the action of dietary DHA on functional recovery after brain trauma. Neuroscience. 2013;248:655–663. doi: 10.1016/j.neuroscience.2013.06.041.
    1. Griesbach G. S., Hovda D. A., Molteni R., Wu A., Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004;125(1):129–139. doi: 10.1016/j.neuroscience.2004.01.030.
    1. Crane A. T., Fink K. D., Smith J. S. The effects of acute voluntary wheel running on recovery of function following medial frontal cortical contusions in rats. Restorative Neurology and Neuroscience. 2012;30(4):325–333. doi: 10.3233/rnn-2012-120232.
    1. Luo C. X., Jiang J., Zhou Q. G., et al. Voluntary exercise-induced neurogenesis in the postischemic dentate gyrus is associated with spatial memory recovery from stroke. Journal of Neuroscience Research. 2007;85(8):1637–1646.
    1. Griesbach G. S., Hovda D. A., Gomez-Pinilla F. Exercise-induced improvement in cognitive performance after traumatic brain injury in rats is dependent on BDNF activation. Brain Research. 2009;1288:105–115. doi: 10.1016/j.brainres.2009.06.045.
    1. Wong-Goodrich S. J. E., Pfau M. L., Flores C. T., Fraser J. A., Williams C. L., Jones L. W. Voluntary running prevents progressive memory decline and increases adult hippocampal neurogenesis and growth factor expression after whole-brain irradiation. Cancer Research. 2010;70(22):9329–9338. doi: 10.1158/0008-5472.can-10-1854.
    1. Winocur G., Becker S., Luu P., Rosenzweig S., Wojtowicz J. M. Adult hippocampal neurogenesis and memory interference. Behavioural Brain Research. 2012;227(2):464–469. doi: 10.1016/j.bbr.2011.05.032.
    1. Clark P. J., Brzezinska W. J., Thomas M. W., Ryzhenko N. A., Toshkov S. A., Rhodes J. S. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience. 2008;155(4):1048–1058. doi: 10.1016/j.neuroscience.2008.06.051.
    1. Itoh T., Imano M., Nishida S., et al. Exercise inhibits neuronal apoptosis and improves cerebral function following rat traumatic brain injury. Journal of Neural Transmission. 2011;118(9):1263–1272. doi: 10.1007/s00702-011-0629-2.
    1. Cechetti F., Worm P. V., Elsner V. R., et al. Forced treadmill exercise prevents oxidative stress and memory deficits following chronic cerebral hypoperfusion in the rat. Neurobiology of Learning and Memory. 2012;97(1):90–96. doi: 10.1016/j.nlm.2011.09.008.
    1. Shih P.-C., Yang Y.-R., Wang R.-Y. Effects of exercise intensity on spatial memory performance and hippocampal synaptic plasticity in transient brain ischemic rats. PLoS ONE. 2013;8(10) doi: 10.1371/journal.pone.0078163.e78163
    1. Shen X., Li A., Zhang Y., et al. The effect of different intensities of treadmill exercise on cognitive function deficit following a severe controlled cortical impact in rats. International Journal of Molecular Sciences. 2013;14(11):21598–21612. doi: 10.3390/ijms141021598.
    1. Hicks R. R., Boggs A., Leider D., et al. Effects of exercise following lateral fluid percussion brain injury in rats. Restorative Neurology and Neuroscience. 1998;12(1):41–47.
    1. Song M.-K., Seon H.-J., Kim I.-G., Han J.-Y., Choi I.-S., Lee S.-G. The effect of combined therapy of exercise and nootropic agent on cognitive function in focal cerebral infarction rat model. Annals of Rehabilitation Medicine. 2012;36(3):303–310. doi: 10.5535/arm.2012.36.3.303.
    1. de Araujo F. L. B., Bertolino G., Funayama C. A. R., Coimbra N. C., de Araujo J. E. Influence of treadmill training on motor performance and organization of exploratory behavior in Meriones unguiculatus with unilateral ischemic stroke: histological correlates in hippocampal CA1 region and the neostriatum. Neuroscience Letters. 2008;431(2):179–183. doi: 10.1016/j.neulet.2007.11.038.
    1. Sim Y.-J., Kim S.-S., Kim J.-Y., Shin M.-S., Kim C.-J. Treadmill exercise improves short-term memory by suppressing ischemia-induced apoptosis of neuronal cells in gerbils. Neuroscience Letters. 2004;372(3):256–261. doi: 10.1016/j.neulet.2004.09.060.
    1. Sim Y.-J., Kim H., Kim J.-Y., et al. Long-term treadmill exercise overcomes ischemia-induced apoptotic neuronal cell death in gerbils. Physiology & Behavior. 2005;84(5):733–738. doi: 10.1016/j.physbeh.2005.02.019.
    1. Chen L., Gong S., Shan L.-D., et al. Effects of exercise on neurogenesis in the dentate gyrus and ability of learning and memory after hippocampus lesion in adult rats. Neuroscience Bulletin. 2006;22(1):1–6.
    1. Kim D.-H., Ko I.-G., Kim B.-K., et al. Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiology & Behavior. 2010;101(5):660–665. doi: 10.1016/j.physbeh.2010.09.021.
    1. Chen M. F., Huang T. Y., Kuo Y. M., Yu L., Chen H. I., Jen C. J. Early postinjury exercise reverses memory deficits and retards the progression of closed-head injury in mice. Journal of Physiology. 2013;591(4):985–1000. doi: 10.1113/jphysiol.2012.241125.
    1. 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 occlusion in rats. Behavioural Brain Research. 2013;243(1):21–27. doi: 10.1016/j.bbr.2012.12.018.
    1. Phillips C., Baktir M. A., Srivatsan M., Salehi A. Neuroprotective effects of physical activity on the brain: a closer look at trophic factor signaling. Frontiers in Cellular Neuroscience. 2014;8, article 170 doi: 10.3389/fncel.2014.00170.
    1. Griesbach G. S., Tio D. L., Vincelli J., McArthur D. L., Taylor A. N. Differential effects of voluntary and forced exercise on stress responses after traumatic brain injury. Journal of Neurotrauma. 2012;29(7):1426–1433. doi: 10.1089/neu.2011.2229.
    1. Griesbach G. S., Tio D. L., Nair S., Hovda D. A. Recovery of stress response coincides with responsiveness to voluntary exercise after traumatic brain injury. Journal of Neurotrauma. 2014;31(7):674–682. doi: 10.1089/neu.2013.3151.
    1. Griesbach G. S., Hovda D. A., Gomez-Pinilla F., Sutton R. L. Voluntary exercise or amphetamine treatment, but not the combination, increases hippocampal brain-derived neurotrophic factor and synapsin I following cortical contusion injury in rats. Neuroscience. 2008;154(2):530–540. doi: 10.1016/j.neuroscience.2008.04.003.
    1. Chang H.-C., Yang Y.-R., Wang S.-G. P., Wang R.-Y. Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion. Behavioural Brain Research. 2009;205(2):450–455. doi: 10.1016/j.bbr.2009.07.033.
    1. Chen J., Qin J., Su Q., Liu Z., Yang J. Treadmill rehabilitation treatment enhanced BDNF-TrkB but not NGF-TrkA signaling in a mouse intracerebral hemorrhage model. Neuroscience Letters. 2012;529(1):28–32. doi: 10.1016/j.neulet.2012.09.021.
    1. Zhang Q.-W., Deng X.-X., Sun X., Xu J.-X., Sun F.-Y. Exercise promotes axon regeneration of newborn striatonigral and corticonigral projection neurons in rats after ischemic stroke. PLoS ONE. 2013;8(11) doi: 10.1371/journal.pone.0080139.e80139
    1. Ploughman M., Granter-Button S., Chernenko G., Tucker B. A., Mearow K. M., 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(4):991–1001. doi: 10.1016/j.neuroscience.2005.08.037.
    1. Ploughman M., Granter-Button S., Chernenko G., et al. Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Research. 2007;1150(1):207–216. doi: 10.1016/j.brainres.2007.02.065.
    1. Griesbach G. S., Gómez-Pinilla F., Hovda D. A. Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. Journal of Neurotrauma. 2007;24(7):1161–1171. doi: 10.1089/neu.2006.0255.
    1. Stranahan A. M., Khalil D., Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nature Neuroscience. 2006;9(4):526–533. doi: 10.1038/nn1668.
    1. Leasure J. L., Decker L. Social isolation prevents exercise-induced proliferation of hippocampal progenitor cells in female rats. Hippocampus. 2009;19(10):907–912. doi: 10.1002/hipo.20563.
    1. Berry A., Bellisario V., Capoccia S., et al. Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice. Psychoneuroendocrinology. 2012;37(6):762–772. doi: 10.1016/j.psyneuen.2011.09.007.
    1. Haast R. A. M., Gustafson D. R., Kiliaan A. J. Sex differences in stroke. Journal of Cerebral Blood Flow and Metabolism. 2012;32(12):2100–2107. doi: 10.1038/jcbfm.2012.141.
    1. Liu M., Kelley M. H., Herson P. S., Hurn P. D. Neuroprotection of sex steroids. Minerva Endocrinologica. 2010;35(2):127–143.
    1. Murphy S. J., McCullough L. D., Smith J. M. Stroke in the female: role of biological sex and estrogen. ILAR Journal. 2004;45(2):147–159. doi: 10.1093/ilar.45.2.147.
    1. Bramlett H. M., Dietrich W. D. Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. Journal of Cerebral Blood Flow and Metabolism. 2004;24(2):133–150.
    1. Tan A. A., Quigley A., Smith D. C., Hoane M. R. Strain differences in response to traumatic brain injury in Long-Evans compared to Sprague-Dawley rats. Journal of Neurotrauma. 2009;26(4):539–548. doi: 10.1089/neu.2008.0611.
    1. Reid W. M., Rolfe A., Register D., Levasseur J. E., Churn S. B., Sun D. Strain-related differences after experimental traumatic brain injury in rats. Journal of Neurotrauma. 2010;27(7):1243–1253. doi: 10.1089/neu.2010.1270.
    1. Markgraf C. G., Kraydieh S., Prado R., Watson B. D., Dietrich W. D., Ginsberg M. D. Comparative histopathologic consequences of photothrombotic occlusion of the distal middle cerebral artery in Sprague-Dawley and Wistar rats. Stroke. 1993;24(2):286–292. doi: 10.1161/01.str.24.2.286.
    1. Herz R. C. G., Gaillard P. J., de Wildt D. J., Versteeg D. H. G. Differences in striatal extracellular amino acid concentrations between Wistar and Fischer 344 rats after middle cerebral artery occlusion. Brain Research. 1996;715(1-2):163–171. doi: 10.1016/0006-8993(95)01572-8.
    1. van der Staay F. J., Augstein K.-H., Horváth E. Sensorimotor impairments in rats with cerebral infarction, induced by unilateral occlusion of the left middle cerebral artery: strain differences and effects of the occlusion site. Brain Research. 1996;735(2):271–284. doi: 10.1016/0006-8993(96)00607-5.
    1. McLin J. P., Steward O. Comparison of seizure phenotype and neurodegeneration induced by systemic kainic acid in inbred, outbred, and hybrid mouse strains. European Journal of Neuroscience. 2006;24(8):2191–2202. doi: 10.1111/j.1460-9568.2006.05111.x.
    1. Fuzik J., Gellért L., Oláh G., et al. Fundamental interstrain differences in cortical activity between Wistar and Sprague-Dawley rats during global ischemia. Neuroscience. 2013;228:371–381. doi: 10.1016/j.neuroscience.2012.10.042.
    1. Al Nimer F., Lindblom R., Ström M., et al. Strain influences on inflammatory pathway activation, cell infiltration and complement cascade after traumatic brain injury in the rat. Brain, Behavior, and Immunity. 2013;27(1):109–122. doi: 10.1016/j.bbi.2012.10.002.
    1. Fox G. B., Levasseur R. A., Faden A. I. Behavioral responses of C57BL/6, FVB/N, and 129/SvEMS mouse strains to traumatic brain injury: implications for gene targeting approaches to neurotrauma. Journal of Neurotrauma. 1999;16(5):377–389. doi: 10.1089/neu.1999.16.377.
    1. Yang G., Kitagawa K., Matsushita K., et al. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Research. 1997;752(1-2):209–218. doi: 10.1016/s0006-8993(96)01453-9.
    1. Schroeter M., Küry P., Jander S. Inflammatory gene expression in focal cortical brain ischemia: differences between rats and mice. Molecular Brain Research. 2003;117(1):1–7. doi: 10.1016/s0169-328x(03)00255-9.
    1. D'Abbondanza J. A., Lass E., Ai J., Macdonald R. L. Neurovascular Events After Subarachnoid Hemorrhage. Vol. 120. Cham, Switzerland: Springer; 2015. Mouse genetic background is associated with variation in secondary complications after subarachnoid hemorrhage; pp. 29–33. (Acta Neurochirurgica Supplement).
    1. Majid A., He Y. Y., Gidday J. M., et al. Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke. 2000;31(11):2707–2714. doi: 10.1161/01.STR.31.11.2707.
    1. Bardutzky J., Shen Q., Henninger N., Bouley J., Duong T. Q., Fisher M. Differences in ischemic lesion evolution in different rat strains using diffusion and perfusion imaging. Stroke. 2005;36(9):2000–2005. doi: 10.1161/01.str.0000177486.85508.4d.
    1. Fujii M., Hara H., Meng W., Vonsattel J. P., Huang Z., Moskowitz M. A. Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57Black/6 mice. Stroke. 1997;28(9):1805–1811. doi: 10.1161/01.str.28.9.1805.
    1. Marosi M., Rákos G., Robotka H., et al. Hippocampal (CA1) activities in Wistar rats from different vendors. Fundamental differences in acute ischemia. Journal of Neuroscience Methods. 2006;156(1-2):231–235. doi: 10.1016/j.jneumeth.2006.03.010.
    1. Oliff H. S., Weber E., Eilon G., Marek P. The role of strain/vendor differences on the outcome of focal ischemia induced by intraluminal middle cerebral artery occlusion in the rat. Brain Research. 1995;675(1-2):20–26. doi: 10.1016/0006-8993(95)00033-m.
    1. Oliff H. S., Weber E., Miyazaki B., Marek P. Infarct volume varies with rat strain and vendor in focal cerebral ischemia induced by transcranial middle cerebral artery occlusion. Brain Research. 1995;699(2):329–331. doi: 10.1016/0006-8993(95)01045-w.
    1. Malá H., Rodríguez Castro M., Pearce H., et al. Delayed intensive acquisition training alleviates the lesion-induced place learning deficits after fimbria-fornix transection in the rat. Brain Research. 2012;1445:40–51. doi: 10.1016/j.brainres.2012.01.035.
    1. Mogensen J., Christensen L. H., Johansson A., Wörtwein G., Bang L. E., Holm S. Place learning in scopolamine-treated rats: the roles of distal cues and catecholaminergic mediation. Neurobiology of Learning and Memory. 2002;78(1):139–166. doi: 10.1006/nlme.2001.4055.
    1. Wörtwein G., Saerup L. H., Charlottenfeld-Starpov D., Mogensen J. Place learning by fimbria-fornix transected rats in a modified water maze. International Journal of Neuroscience. 1995;82(1-2):71–81. doi: 10.3109/00207459508994291.
    1. Mogensen J., Pedersen T. K., Holm S., Bang L. E. Prefrontal cortical mediation of rats' place learning in a modified water maze. Brain Research Bulletin. 1995;38(5):425–434. doi: 10.1016/0361-9230(95)02009-g.
    1. Wilms I., Mogensen J. Dissimilar outcomes of apparently similar procedures as a challenge to clinical neurorehabilitation and basic research: when the same is not the same. Neurorehabilitation. 2011;29(3):221–227. doi: 10.3233/nre-2011-0696.
    1. Mogensen J. Animal models in neuroscience. In: Hau J., Schapiro S. J., editors. Handbook of Laboratory Animal Science, Volume II. Animal Models. CRC Press; 2011. pp. 47–73.
    1. Jorge R. E., Arciniegas D. B. Mood disorders after TBI. Psychiatric Clinics of North America. 2014;37(1):13–29. doi: 10.1016/j.psc.2013.11.005.
    1. Austin M.-P., Mitchell P., Goodwin G. M. Cognitive deficits in depression: possible implications for functional neuropathology. British Journal of Psychiatry. 2001;178:200–206. doi: 10.1192/bjp.178.3.200.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren