Publicado
Caracterización temporo-espacial del patrón de marcha en roedores como modelo animal de lesión cerebral cerebrovascular
Temporal and Spatial Characterization of Gait Pattern in Rodents as an Animal model of Cerebrovascular Lesion
DOI:
https://doi.org/10.15446/abc.v22n3.65244Palabras clave:
accidente cerebrovascular, actividad motora, análisis de la marcha, pruebas funcionales, roedores. (es)functional testing, gait analysis, motor activity, rodents, stroke. (en)
Descargas
En la investigación sobre movimiento, la experimentación animal ha proporcionado fundamentación científica para la investigación clínica, mejorando procedimientos diagnósticos y de rehabilitación. Lesiones cerebrales en roedores pueden ser usadas para modelar síntomas locomotores, sensoriales y/o cognitivos. Con el propósito de determinar la funcionalidad locomotriz y sensorial en roedores, se han propuesto varios métodos de evaluación y pronóstico clínico para identificar y evaluar adaptaciones estructurales y mecanismos de neuro-recuperación. Esto ha permitido que métodos de intervención terapéutica, como el ejercicio físico, sean utilizados para restaurar funciones sensitivo-motoras y cognitivas en roedores y humanos. La extrapolación (translación) de los resultados de investigaciones en ciencias básicas a áreas clínicas supone la continua cooperación y retroalimentación entre investigadores y profesionales de la salud, favoreciendo la formulación de intervenciones terapéuticas más eficaces basadas en resultados obtenidos de la experimentación animal. El objetivo de esta revisión es exponer las principales deficiencias motoras y los métodos empleados para determinar la dificultad motriz en la marcha en roedores con lesión cerebrovascular, para lo cual se realizó una revisión de literatura, sobre términos definidos (MeSH), en las bases de datos PsychINFO, Medline y Web of Science, entre enero de 2000 y enero de 2017. Se excluyeron artículos de carácter cualitativo o narrativo, sin revisión por pares, disertaciones, tesis o trabajos de grado y resúmenes de conferencias. Se revisan algunas manifestaciones clínicas, su efecto en la locomotricidad en roedores, algunas metodologías usadas para generar lesiones y para estudiar la función motriz, los principales métodos de medición y algunos aspectos translacionales.
Animal experimentation is crucial for the advance in the understanding of pathophysiological mechanisms and their application on both clinical diagnosis and neuro-rehabilitation. Particularly, rodent brain lesion is commonly used in the modeling of locomotor, somatosensory and cognitive symptoms. The automated rodent gait analysis has been proposed as a tool for studying locomotor and sensory abilities and its use includes the identification of functional alterations, structural adaptations as well as neuro-rehabilitation mechanisms. From that standpoint, the effectiveness of many therapeutic intervention (i.e. physical exercises) has been documented in rodents and humans. The translation from experimental data to clinical conditions requires the continuous collaboration and feedback between researchers and health clinicians looking for the selection of the best rehabilitation protocols obtained from animal research. Here we will show some locomotor alterations, the traditional methods used to assess motor dysfunction and gait abnormalities in rodent models with stroke. The aim of this review is to show some motor deficiencies and some methods used to establish gait disturbances in rodents with cerebrovascular lesion. The review included the search of defined terms (MeSH) in PychINFO, Medline and Web of Science, between January 2000 and January 2017. Qualitative and narrative reports, dissertations, end course works and conference resumes were discarded. The review focuses on some clinical signs, their effects on rodent locomotor activity, some methodologies used to create lesion and to study motor function, some assessment methods and some translational aspects.
Referencias
Acevedo-Triana CA, Ávila-Campos JE, Cardenas FP. Effects of exercise and motor activity on both functions and brain structure. Rev Mex Neurocience. 2014;15(1):36–53.
Agca C, Fritz JJ, Walker LC, Levey AI, Chan AW, Lah JJ, et al. Development of transgenic rats producing human beta-amyloid precursor protein as a model for Alzheimer’s disease: transgene and endogenous APP genes are regulated tissue-specifically. BMC Neurosci. 2008;9:28. Doi:10.1186/1471-2202-9-28
Allen JL, Kautz SA, Neptune RR. Step length asymmetry is representative of compensatory mechanisms used in post-stroke hemiparetic walking. Gait Posture. 2011;33(4):538-543. Doi:10.1016/j.gaitpost.2011.01.004
Allred RP, Adkins DL, Woodlee MT, Husbands LC, Maldonado MA, Kane JR, et al. The Vermicelli Handling Test: A simple quantitative measure of dexterous forepaw function in rats. J Neurosci Methods. 2008;170(2):229-244.
Bacigaluppi M, Comi G, Hermann DM. Animal models of ischemic stroke. Part two: modeling cerebral ischemia. Open Neurol J. 2010;4:34-38. Doi:10.2174/1874205X01004020034
Balaban B, Tok F. Gait disturbances in patients with stroke. PM R. 2014;6(7):635-642.
Bales HW. Neurocysticercosis: migration of a parasite. J Am Acad Nurse Pract. 2000;12(6):240-248.
Ballermann M, Metz GA, McKenna JE, Klassen F, Whishaw IQ. The pasta matrix reaching task: a simple test for measuring skilled reaching distance, direction, and dexterity in rats. J Neurosci Methods. 2001;106(1):39-45.
Barbosa EH, Vallim JH, Lachat J-J, de Castro VLSS. Assessments of motor abnormalities on the grid-walking and foot-fault tests from undernutrition in wistar rats. J Mot Behav. 2016;48(1):5-12.
Barros M, Tomaz C. Non-human primate models for investigating fear and anxiety. Neurosci Biobehav Rev. 2002;26(2):187-201.
Baumans V. Science-based assessment of animal welfare: laboratory animals. Rev Sci Tech. 2005;24(2):503-513.
Beare JE, Morehouse JR, DeVries WH, Enzmann GU, Burke DA, Magnuson DSK, et al. Gait Analysis in normal and spinal contused mice using the treadscan system. J Neurotrauma. 2009;26(11):2045-2056.
Beck MH, Haumesser JK, Kuhn J, Altschuler J, Kuhn AA, van Riesen C. Short- and long-term dopamine depletion causes enhanced beta oscillations in the cortico-basal ganglia loop of parkinsonian rats. Exp
Neurol. United States. 2016;286:124-136. Doi:10.1016/j.expneurol.2016.10.005
Berryman ER, Harris RL, Moalli M, Bagi CM. Digigait??? quantitation of gait dynamics in rat rheumatoid arthritis model. J Musculoskelet Neuronal Interact. 2009;9(2):89-98.
Biernaskie J, Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci. 2001;21(14):5272-5280.
Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P, et al. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc. 2009;4(10):1560-1564.
Brevetti LS, Chang DS, Tang GL, Sarkar R, Messina LM. Overexpression of endothelial nitric oxide synthase increases skeletal muscle blood flow and oxygenation in severe rat hind limb ischemia. J Vasc Surg. 2003;38(4):820-826. Doi:10.1016/S0741-5214(03)00555-X
Brown CE, Aminoltejari K, Erb H, Winship IR, Murphy TH. In Vivo Voltage-Sensitive Dye Imaging in Adult Mice Reveals That Somatosensory Maps Lost to Stroke Are Replaced over Weeks by New Structural and Functional Circuits with Prolonged Modes of Activation within Both the Peri-Infarct Zone and Distant Sites. J Neurosci. 2009;29(6):1719-1734.
Cardenas FP, De Muñoz M, Hernandez JM, Cárdenas MAN. Estimulación eléctrica nerviosa percutánea y entrenamiento aeróbico para rehabilitación de la marcha en ratas con compresión del nervio ciático. Rev Asoc Colomb Fisioter. 2014;55:11-15.
Carmichael ST. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx. 2005;2(3):396-409.
Casals JB, Pieri NCG, Feitosa MLT, Ercolin ACM, Roballo KCS, Barreto RSN, et al. The use of animal models for stroke research: A review. Comp Med. 2011;61(4):305-313.
Cassilhas RC, Lee KS, Venâncio DP, Oliveira MGM, Tufik S, de Mello MT. Resistance exercise improves hippocampus-dependent memory. Brazilian J Med Biol Res = Rev Bras Pesqui medicas e Biol. Associação Brasileira de Divulgação Científica; 2012;45(12):1215-1220.
Doi:10.1590/s0100-879x2012007500138
Cenci MA, Whishaw IQ, Schallert T. Animal models of neurological deficits: how relevant is the rat? Nat Rev Neurosci. 2002;3(7):574-579. Doi:10.1038/nrn877
Chao OY, Pum ME, Li JS, Huston JP. The grid-walking test: Assessment of sensorimotor deficits after moderate or severe dopamine depletion by 6-hydroxydopamine lesions in the dorsal striatum and medial forebrain bundle. Neuroscience. 2012;202:318-325. Doi:10.1016/j.neuroscience.2011.11.016
Coelho BP, Giraldi-Guimarães A. Effect of age and gender on recovery after stroke in rats treated with bone marrow mononuclear cells. Neurosci Res. 2014;88(C):67-73. Doi:10.1016/j.neures.2014.08.007
Cordova CA, Jackson D, Langdon KD, Hewlett KA, Corbett D. Impaired executive function following ischemic stroke in the rat medial prefrontal cortex. Behav Brain Res. 2014;258:106-111. Doi:10.1016/j.bbr.2013.10.022
Dalise S, Ambrosio F, Modo M. Adaptive plasticity and recovery in preclinical models of stroke. Arch Ital Biol. 2015;152(4):190-215. Doi:10.4449/AIB.V152I4.1851
Dehoux J, Gianello P. The importance of large animal models in transplantation. Front Biosci. 2007;12:4864-4880. Doi:10.2741/2434
Dimyan M a, Cohen LG. Neuroplasticity in the context of motor rehabilitation after stroke. Nat Rev Neurol. 2011;7(2):76-85.
Dorman CW, Krug HE, Frizelle SP, Funkenbusch S, Mahowald ML. A comparison of DigigaitTM and TreadscanTM imaging systems: assessment of pain using gait analysis in murine monoarthritis. J Pain Res. 2014;7:25-35.
Drew T, Jiang W, Widajewicz W. Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat. Brain Res Rev. 2002;40(1–3):178-191. Doi:10.1016/S0165-0173(02)00200-X
Durukan A, Tatlisumak T. Acute ischemic stroke: Overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav. 2007;87(1):179-197. Doi:10.1016/j.pbb.2007.04.015
Eftaxiopoulou T, Macdonald W, Britzman D, Bull AMJ. Gait compensations in rats after a temporary nerve palsy quantified using temporo-spatial and kinematic parameters. J Neurosci Methods. 2014;232:16-23. Doi:10.1016/j.jneumeth.2014.04.011
Eng JJ, Tang PF. Gait training strategies to optimize walking ability in people with stroke: A synthesis of the evidence. Expert Rev Neurother. 2007;7(10):1417-1436. Doi:10.1586/14737175.7.10.1417
Engel O, Kolodziej S, Dirnagl U, Prinz V. Modeling stroke in mice - middle cerebral artery occlusion with the filament model. J Vis Exp. 2011;47(47):e2423.
Esposito S, Longo MR. Guillain-Barre syndrome. Autoimmun Rev Netherlands; 2016. Doi:10.1016/j.autrev.2016.09.022
Faherty CJ, Raviie Shepherd K, Herasimtschuk A, Smeyne RJ. Environmental enrichment in adulthood eliminates neuronal death in experimental Parkinsonism. Brain Res Mol Brain Res. 2005;134(1):170-179.
Font MA, Arboix A, Krupinski J. Angiogenesis, neurogenesis and neuroplasticity in ischemic stroke. Curr Cardiol Rev. 2010;6(3):238-244.
Fritz NE, Kegelmeyer DA, Kloos AD, Linder S, Park A, Kataki M, et al. Motor performance differentiates individuals with Lewy body dementia, Parkinson’s and Alzheimer’s disease. Gait Posture. 2016;50:1-7. Doi:10.1016/j.gaitpost.2016.08.009
Gardner AJ, Zafonte R. Neuroepidemiology of traumatic brain injury. Handb Clin Neurol. 2016;138:207-223. Doi:10.1016/B978-0-12-802973-2.00012-4
Gillis GB, Biewener AA. Hindlimb muscle function in relation to speed and gait: in vivo patterns of strain and activation in a hip and knee extensor of the rat (Rattus norvegicus). J Exp Biol. 2001;204(Pt 15):2717-2731.
Goldie PA, Matyas TA, Evans OM. Gait after stroke: Initial deficit and changes in temporal patterns for each gait phase. Arch Phys Med Rehabil. 2001;82(8):1057-1065. Doi:10.1053/apmr.2001.25085
Gottlieb, M., Leal-Campanario, R., Campos-Esparza, M. R., Sánchez-Gómez, M. V., Alberdi, E., Arranz, A. et al. Neuroprotection by two polyphenols following excitotoxicity and experimental ischemia. Neurobiol Dis. 2006;23(2):374-386.
Goutianos G, Tzioura A, Kyparos A, Paschalis V, Margaritelis N V, Veskoukis AS, et al. The rat adequately reflects human responses to exercise in blood biochemical profile: a comparative study. Physiol Rep. 2015;3(2):e12293.
Hamers FP, Lankhorst A J, van Laar TJ, Veldhuis WB, Gispen WH. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma. 2001;18(2):187-201. Doi:10.1089/08977150150502613
Hampton TG, Kale A, Amende I, Tang W, McCue S, Bhagavan HN, et al. Gait Disturbances in Dystrophic Hamsters, Gait Disturbances in Dystrophic Hamsters. BioMed Res Int BioMed Res Int. 2011; 2011:e235354.
Hattori K, Lee H, Hurn PD, Crain BJ, Traystman RJ, DeVries AC. Cognitive deficits after focal cerebral ischemia in mice. Stroke. 2000;31(8):1939-1944.
Hill JW, Nemoto EM. Transient middle cerebral artery occlusion with complete reperfusion in spontaneously hypertensive rats. MethodsX. 2014;1:283-291. Doi:10.1016/j.mex.2014.11.001
Hollman JH, McDade EM, Petersen RC. Normative spatiotemporal gait parameters in older adults. Gait Posture. 2011;34(1):111-118. Doi:10.1016/j.gaitpost.2011.03.024
Hossmann K-A. Pathophysiology and therapy of experimental stroke. Cell Mol Neurobiol. 2006;26(7-8):1057-1083. Doi:10.1007/s10571-006-9008-1
Hua Y, Schallert T, Keep RF, Wu J, Hoff JT, Xi G. Behavioral tests after intracerebral hemorrhage in the rat. Stroke. 2002;33(10):2478-2484. Doi:10.1161/01.STR.0000032302.91894.0F
Jett D A, Kuhlmann A C, Farmer SJ, Guilarte TR. Age-dependent effects of developmental lead exposure on performance in the Morris water maze. Pharmacol Biochem Behav. 2001;57(1-2):271–279.
Johnson VE, Meaney DF, Cullen DK, Smith DH. Animal models of traumatic brain injury. Handb Clin Neurol. 2015;127(2):115-128. Doi:10.1016/B978-0-444-52892-6.00008-8
Jung JE, Kim GS, Chan PH. Neuroprotection by interleukin-6 is mediated by signal transducer and activator of transcription 3 and antioxidative signaling in ischemic stroke. Stroke. 2011;42(12):3574-359. Doi:10.1161/STROKEAHA.111.626648
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(2):e16643. Doi:10.1371/journal.pone.0016643
Kleim JA, Boychuk JA, Adkins DL. Rat models of upper extremity impairment in stroke. ILAR J. 2007;48(4):374–384.
Kluding M, Tseng Y, Billinger A. Exercise and Executive Function in Individuals With Chronic Stroke: A Pilot Study. J Neurol Phys Ther. 2011;35(1):11-18.
Koopmans GC, Deumens R, Brook G, Gerver J, Honig WMM, Hamers FPT, et al. Strain and locomotor speed affect over-ground locomotion in intact rats. Physiol Behav. 2007;92(5):993-1001. Doi:10.1016/j.physbeh.2007.07.018
Koositamongkol S, Sindhu S, Pinyopasakul W, Nilanont Y, Redman RW. Factors influencing functional recovery in patients with acute ischemic stroke. Collegian. 2013;20(4):207-213. Doi:10.1016/j.colegn.2012.09.002
Kucharikova A, Schreiberova A, Zavodska M, Gedrova S, Hricova L, Pavel J, et al. Repeated Baclofen treatment ameliorates motor dysfunction, suppresses reflex activity and decreases the expression of signaling proteins in reticular nuclei and lumbar motoneurons after spinal trauma in rats. Acta Histochem. Germany; 2014;116(2):344-
Doi:10.1016/j.acthis.2013.08.012
Lake EM, Chaudhuri J, Thomason L, Janik R, Ganguly M, Brown M, et al. The Effects of Delayed Reduction of Tonic Inhibition on Ischemic Lesion and Sensorimotor Function. J Cereb Blood Flow Metab. 2015;35(10):1601-1609.
Li L, Rong W, Ke Z, Hu X, Tong K-Y. The effects of training intensities on motor recovery and gait symmetry in a rat model of ischemia. Brain Inj. 2013a;27(4):408-416.
Li S, Shi Z, Zhang H, Liu X, Chen S, Jin J, et al. Assessing gait impairment after permanent middle cerebral artery occlusion in rats using an automated computer-aided control system. Behav Brain Res. 2013b;250:174-191. Doi:10.1016/j.bbr.2013.04.044
Linden J, Van de Beeck L, Plumier J-C, Ferrara A. Procedural learning as a measure of functional impairment in a mouse model of ischemic stroke. Behav Brain Res. 2016;307:35-45.
Lipsanen A, Jolkkonen J. Experimental approaches to study functional recovery following cerebral ischemia. Cell Mol Life Sci. 2011;68(18):3007-3017. Doi:10.1007/s00018-011-0733-3
Liu Y, Ao LJ, Lu G, Leong E, Liu Q, Wang XH, et al. Quantitative gait analysis of long-term locomotion deficits in classical unilateral striatal intracerebral hemorrhage rat model. Behav Brain Res. 2013;257:166-177. Doi:10.1016/j.bbr.2013.10.007
Livingston-Thomas JM, Tasker RA. Animal models of post-ischemic forced use rehabilitation: methods, considerations, and limitations. Exp Transl Stroke Med. 2013;5(1):2.
Luft AR, MacKo RF, Forrester LW, Villagra F, Ivey F, Sorkin JD, et al. Treadmill exercise activates subcortical neural networks and improves walking after stroke: A randomized controlled trial. Stroke. 2008;39(12):3341-3350. Doi:10.1161/STROKEAHA.108.527531
Majid A. Neuroprotection in Stroke: Past, Present, and Future. ISRN Neurol. 2014;2014:1-17.
Malva JO, Rego AC, Cunha RA, Oliveira CR. Interaction between neurons and glia in aging and disease. Interact. Between Neurons Glia Aging Dis. 2007. Doi:10.1007/978-0-387-70830-0
Mang CS, Campbell KL, Ross CJD, Boyd L A. Perspective Promoting Neuroplasticity for Motor Rehabilitation After Stroke: Considering the Effects of Aerobic Brain-Derived Neurotrophic Factor. Phys Ther. 2013;93(12):1707-1716. Doi:10.2522/ptj.20130053
Marin R, Williams A, Hale S, Burge B, Mense M, Bauman R, et al. The effect of voluntary exercise exposure on histological and neurobehavioral outcomes after ischemic brain injury in the rat. Physiol Behav. 2003;80(2-3):167-175. Doi:10.1016/j.physbeh.2003.06.001
Marini C, Russo T, Felzani G. Incidence of stroke in young adults: a review. Stroke Res Treat. 2010;2011:535672.
Martino G, Martino G, Pluchino S, Pluchino S. The therapeutic potential of neural stem cells. Nat Rev Neurosci. 2006;7(May):395-406.
Metz GA, Whishaw IQ. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: A new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods. 2002;115(2):169-179. Doi:10.1016/S0165-0270(02)00012-2
Metz GAS, Dietz V, Schwab ME, Van de Meent H. The effects of unilateral pyramidal tract section on hindlimb motor performance in the rat. Behav Brain Res. 1998;96(1-2):37-46. Doi:10.1016/S0166-4328(97)00195-21
Minami T, Matsumura S, Nishizawa M, Sasaguri Y, Hamanaka N, Ito S. Acute and late effects on induction of allodynia by acromelic acid, a mushroom poison related structurally to kainic acid. Br J Pharmacol. 2004;142(4):679-688.
Mohs C. R., Haroutunian V. Alzheimer disease: From earliest symptoms to end stage. In: Davis KL., Charney D, Coyle JT., Nemeroff C, editors. Neuropsychopharmacology: The Fifth Generation of Progress. American College of Neuropsychopharmacology; 2002. p. 1188-1197.
Montoya CP, Campbell-Hope LJ, Pemberton KD, Dunnett SB. The “staircase test”: a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods. 1991;36(2-3):219-328. Doi:10.1016/0165-0270(91)90048-5
Nielsen RK, Samson KL, Simonsen D, Jensen W. Effect of early and late rehabilitation onset in a chronic rat model of ischemic stroke-assessment of motor cortex signaling and gait functionality over time. IEEE Trans Neural Syst Rehabil Eng. 2013;21(6):1006-1015. Doi:10.1109/TNSRE.2013.2279375
Ostrovskaya RU, Romanova GA, Barskov I V, Shanina E V, Gudasheva TA, Victorov I V, et al. Memory restoring and neuroprotective effects of the proline-containing dipeptide, GVS-111, in a photochemical stroke model. Behav Pharmacol. 1999;10(5):549-553.
Ozolins B, Aimers N, Parrington L, Pearce AJ. Movement disorders and motor impairments following repeated head trauma: A systematic review of the literature 1990-2015. Brain Inj. England; 2016;30(8):937-947. Doi:10.3109/02699052.2016.1147080
Parker AJ, Clarke KA. Gait topography in rat locomotion. Physiol Behav. 1990;48(1):41-47. Doi:10.1016/0031-9384(90)90258-6
Parkkinen S, Ortega FJ, Kuptsova K, Huttunen J, Tarkka I, Jolkkonen J. Gait impairment in a rat model of focal cerebral ischemia. Stroke Res Treat. 2013;2013:e410972. Doi:10.1155/2013/410972
Pin-Barre C, Laurin J. Physical Exercise as a Diagnostic, Rehabilitation, and Preventive Tool: Influence on Neuroplasticity and Motor Recovery after Stroke. Neural Plast. 2015;2015:e608581. Doi:10.1155/2015/608581
Pulsinelli, W.A., Brierley, J.B. A new model of bilateral hemispheric ischemia in the unanesthetized rat. Stroke 1979;10:267-272
Rasmussen RS, Overgaard K, Hildebrandt-Eriksen ES, Boysen G. d-Amphetamine improves cognitive deficits and physical therapy promotes fine motor rehabilitation in a rat embolic stroke model. Acta Neurol Scand. 2006;113(3):189-198.
Rattka M, Fluri F, Krstić M, Asan E, Volkmann J. A Novel Approach to Assess Motor Outcome of Deep Brain Stimulation Effects in the Hemiparkinsonian Rat: Staircase and Cylinder Test. J Vis Exp. 2016.
Reger ML, Hovda DA, Giza CC. Ontogeny of rat recognition memory measured by the novel object recognition task. Dev Psychobiol. 2009;51(8):672-678. Doi:10.1002/dev.20402
Richter A. The Genetically Dystonic Hamster: An Animal Model of Paroxysmal Dystonia. J Child Neurol. 2005.
Rinalduzzi S, Serafini M, Capozza M, Accornero N, Missori P, Trompetto C, et al. Stance Postural Strategies in Patients with Chronic Inflammatory Demyelinating Polyradiculoneuropathy. PLoS One. 2016;11(3):e0151629. Doi:10.1371/journal.pone.0151629
Russell JC, Proctor SD. Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis. Cardiovasc Pathol. 2006;15(6):318-330. Doi:10.1016/j.carpath.2006.09.001
Sarkaki A, Rezaiei M, Gharibnaseri MK, Rafieirad M. Improving active and passive avoidance memories deficits due to permanent cerebral ischemia by pomegranate seed extract in female rats. Malaysian J Med Sci. 2013;20(2):26-35.
Schaar KL, Brenneman MM, Savitz SI. Functional assessments in the rodent stroke model. Exp Transl Stroke Med. 2010;2(1):13.
Scheidtmann K, Fries W, Müller F, Koenig E. Effect of levodopa in combination with physiotherapy on functional motor recovery after stroke: A prospective, randomised, double-blind study. Lancet. 2001;358(9284):787-790. Doi:10.1016/S0140-6736(01)05966-9
Scherder E, Eggermont L, Sergeant J, Boersma F. Physical activity and cognition in Alzheimer’s disease: relationship to vascular risk factors, executive functions and gait. Rev Neurosci. 2007;18(2):149-158.
Schuch CP, Jeffers MS, Antonescu S, Nguemeni C, Gomez-Smith M, Pereira LO, et al. Enriched rehabilitation promotes motor recovery in rats exposed to neonatal hypoxia-ischemia. Behav Brain Res. 2016; 304:42-50.
Siegmund A, Wotjak CT. Hyperarousal does not depend on trauma-related contextual memory in an animal model of Posttraumatic Stress Disorder. Physiol Behav. 2007;90(1):103-107.
Sierra C, Coca A, Schiffrin EL. Vascular mechanisms in the pathogenesis of stroke. Curr Hypertens Rep. 2011;13(3):200-207. Doi:10.1007/s11906-011-0195-x
Simjee SU, Jawed H, Quadri J, Saeed SA. Quantitative gait analysis as a method to assess mechanical hyperalgesia modulated by disease-modifying antirheumatoid drugs in the adjuvant-induced arthritic rat. Arthritis Res Ther. 2007;9(5):R91.
Sironi, L., Cimino, M., Guerrini, U., Calvio, A. M., Lodetti, B., Asdente, M., et al. Treatment with statins after induction of focal ischemia in rats reduces the extent of brain damage. Arterioscler Thromb Vasc Biol. 2003;23(2):322-327.
Spires TL, Hannan AJ. Nature, nurture and neurology: gene-environment interactions in neurodegenerative disease. FEBS Anniversary Prize Lecture delivered on 27 June 2004 at the 29th FEBS Congress in Warsaw. FEBS J . 2005;272(10):2347-2361.
Sughrue ME, Mocco J, Komotar RJ, Mehra A, D’Ambrosio AL, Grobelny BT, et al. An improved test of neurological dysfunction following transient focal cerebral ischemia in rats. J Neurosci Methods. 2006;151(2):83-89. Doi:10.1016/j.jneumeth.2005.04.023
Tamura, A., Graham, D.I., McCullogh, J., Teasdale, M.G. Focal cerebral schemia in the rat: 1: description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cereb Blood Flow Metab. 1981;1:53-60.
Tennant K, Asay AL, Allred RP, Ozburn AR, Kleim J, Jones T. The vermicelli and capellini handling tests: simple quantitative measures of dexterous forepaw function in rats and mice. J Vis Exp. 2010(41):1-6. Doi:10.3791/2076
Titianova EB, Peurala SH, Pitkänen K, Tarkka IM. Gait reveals bilateral adaptation of motor control in patients with chronic unilateral stroke. Aging Clin Exp Res. 2008;20(2):131-138.
Vandamme TF. Use of rodents as models of human diseases. J Pharm Bioallied Sci. 2014;6(1):2-9.
Vandeputte C, Taymans J-M, Casteels C, Coun F, Ni Y, Van Laere K, et al. Automated quantitative gait analysis in animal models of movement disorders. BMC Neurosci. 2010;11:92.
Vaysse L, Conchou F, Demain B, Davoust C, Plas B, Ruggieri C, et al. Strength and fine dexterity recovery profiles after a primary motor cortex insult and effect of a neuronal cell graft. Behav Neurosci. 2015;129(4):423–434.
Vorhees C V, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848-858.
Wang XH, Lu G, Hu X, Tsang KS, Kwong WH, Wu FX, et al. Quantitative assessment of gait and neurochemical correlation in a classical murine model of Parkinson’s disease. BMC Neurosci. 2012;13:142.
Wang Y, Bontempi B, Hong SM, Mehta K, Weinstein PR, Abrams GM, et al. A comprehensive analysis of gait impairment after experimental stroke and the therapeutic effect of environmental enrichment in rats. J Cereb Blood Flow Metab. 2008;28(12):1936-1950.
Wang-Fischer Y, Prado R, Koetzner L. Manual of Stroke Models in Rats. Anat. Cereb. Circ. Rat. CRC Press; 2008. Doi:10.1201/9781420009521
Westerga J, Gramsbergen A. The development of locomotion in the rat. Brain Res Dev Brain Res. 1990;57(2):163-174.
Witt BJ, Gami AS, Ballman K V., Brown RD, Meverden RA, Jacobsen SJ, et al. The Incidence of Ischemic Stroke in Chronic Heart Failure: A Meta-Analysis. J Card Fail. 2007;13(6):489-496. Doi:10.1016/j.cardfail.2007.01.009
Yu J, Zhu H, Gattoni-Celli S, Taheri S, Kindy MS. Dietary supplementation of GrandFusion ® mitigates cerebral ischemia-induced neuronal damage and attenuates inflammation. Nutr Neurosci. 2016;19(7):290-300.
Zhou M, Zhang W, Chang J, Wang J, Zheng W, Yang Y, et al. Gait analysis in three different 6-hydroxydopamine rat models of Parkinson’s disease. Neurosci Lett. 2015;584:184-189. Doi:10.1016/j.neulet.2014.10.032
Dimensions
PlumX
Visitas a la página del resumen del artículo
Descargas
Cómo citar
Licencia
Derechos de autor 2017 Acta Biológica Colombiana
Esta obra está bajo una licencia internacional Creative Commons Atribución 4.0.
1. La aceptación de manuscritos por parte de la revista implicará, además de su edición electrónica de acceso abierto bajo licencia Attribution-NonCommercial-ShareAlike 4.0 (CC BY NC SA), la inclusión y difusión del texto completo a través del repositorio institucional de la Universidad Nacional de Colombia y en todas aquellas bases de datos especializadas que el editor considere adecuadas para su indización con miras a incrementar la visibilidad de la revista.
2. Acta Biológica Colombiana permite a los autores archivar, descargar y compartir, la versión final publicada, así como las versiones pre-print y post-print incluyendo un encabezado con la referencia bibliográfica del articulo publicado.
3. Los autores/as podrán adoptar otros acuerdos de licencia no exclusiva de distribución de la versión de la obra publicada (p. ej.: depositarla en un archivo telemático institucional o publicarla en un volumen monográfico) siempre que se indique la publicación inicial en esta revista.
4. Se permite y recomienda a los autores/as difundir su obra a través de Internet (p. ej.: en archivos institucionales, en su página web o en redes sociales cientificas como Academia, Researchgate; Mendelay) lo cual puede producir intercambios interesantes y aumentar las citas de la obra publicada. (Véase El efecto del acceso abierto).
