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Published in: BMC Neurology 1/2017

Open Access 01-12-2017 | Research article

Comprehensive catwalk gait analysis in a chronic model of multiple sclerosis subjected to treadmill exercise training

Authors: Danielle Bernardes, Alexandre Leite Rodrigues Oliveira

Published in: BMC Neurology | Issue 1/2017

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Abstract

Background

Multiple sclerosis (MS) is a demyelinating disease with a wide range of symptoms including walking impairment and neuropathic pain mainly represented by mechanical allodynia. Noteworthy, exercise preconditioning may affect both walking impairment and mechanical allodynia. Most of MS symptoms can be reproduced in the animal model named experimental autoimmune encephalomyelitis (EAE). Usually, neurological deficits of EAE are recorded using a clinical scale based on the development of disease severity that characterizes tail and limb paralysis. Following paralysis recovery, subtle motor alterations and even mechanical allodynia investigation are difficult to record, representing sequels of peak disease. The aim of the present study was to investigate the walking dysfunction by the catwalk system (CT) in exercised and non-exercised C57BL/6 mice submitted to EAE with MOG35–55 up to 42 days post-induction (dpi).

Methods

Twenty-four C57BL/6 female mice were randomly assigned to unexercised (n = 12) or exercised (n = 12) groups. The MOG35–55 induced EAE model has been performed at the beginning of the fifth week of the physical exercise training protocol. In order to characterize the gait parameters, we used the CT system software version XT 10.1 (Noldus Inc., The Netherlands) from a basal time point (before induction) to 42 days post induction (dpi). Statistical analyses were performed with GraphPad Prisma 4.0 software.

Results

Data show dynamic gait changes in EAE mice including differential front (FP) and hind paw (HP) contact latency. Such findings are hypothesized as related to an attempt to maintain balance and posture similar to what has been observed in patients with MS. Importantly, pre-exercised mice show differences in the mentioned gait compensation, particularly at the propulsion sub-phase of HP stand. Besides, we observed reduced intensity of the paw prints as well as reduced print area in EAE subjects, suggestive of a development of chronic mechanical allodynia in spite of being previously exercised.

Conclusions

Our data suggest that Catwalk system is a useful tool to investigate subtle motor impairment and mechanical allodynia at chronic time points of the EAE model, improving the functional investigation of gait abnormalities and demyelination sequelae.
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Literature
1.
go back to reference Loleit V, Biberacher V, Hemmer B. Current and future therapies targeting the immune system in multiple sclerosis. Curr Pharm Biotechnol. 2014;15:276–96.CrossRefPubMed Loleit V, Biberacher V, Hemmer B. Current and future therapies targeting the immune system in multiple sclerosis. Curr Pharm Biotechnol. 2014;15:276–96.CrossRefPubMed
2.
go back to reference Bagnato F, Centonze D, Galgani S, Grasso MG, Haggiag S, Strano S. Painful and involuntary multiple sclerosis. Expert Opin Pharmacother. 2011;12:763–77.CrossRefPubMedPubMedCentral Bagnato F, Centonze D, Galgani S, Grasso MG, Haggiag S, Strano S. Painful and involuntary multiple sclerosis. Expert Opin Pharmacother. 2011;12:763–77.CrossRefPubMedPubMedCentral
3.
go back to reference Doshi A, Chataway J. Multiple sclerosis, a treatable disease. Clin Med (Northfield Il). 2016;16:53–9.CrossRef Doshi A, Chataway J. Multiple sclerosis, a treatable disease. Clin Med (Northfield Il). 2016;16:53–9.CrossRef
4.
go back to reference Motl RW, Goldman MD, Benedict RHB. Walking impairment in patients with multiple sclerosis: exercise training as a treatment option. Neuropsychiatr Dis Treat. 2010;6:767–74.CrossRefPubMedPubMedCentral Motl RW, Goldman MD, Benedict RHB. Walking impairment in patients with multiple sclerosis: exercise training as a treatment option. Neuropsychiatr Dis Treat. 2010;6:767–74.CrossRefPubMedPubMedCentral
5.
go back to reference Comber L, Galvin R, Coote S. Gait deficits in people with multiple sclerosis: a systematic review and meta-analysis. Gait Posture. 2017;51:25–35.CrossRefPubMed Comber L, Galvin R, Coote S. Gait deficits in people with multiple sclerosis: a systematic review and meta-analysis. Gait Posture. 2017;51:25–35.CrossRefPubMed
6.
go back to reference Foley PL, Vesterinen HM, Laird BJ, Sena ES, Colvin LA, Chandran S, et al. Prevalence and natural history of pain in adults with multiple sclerosis: systematic review and meta-analysis. Pain. 2013;154:632–42.CrossRefPubMed Foley PL, Vesterinen HM, Laird BJ, Sena ES, Colvin LA, Chandran S, et al. Prevalence and natural history of pain in adults with multiple sclerosis: systematic review and meta-analysis. Pain. 2013;154:632–42.CrossRefPubMed
7.
go back to reference Vrinten DH, Hamers FFT. “CatWalk” automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; a comparison with von Frey testing. Pain. 2003;102:203–9.CrossRefPubMed Vrinten DH, Hamers FFT. “CatWalk” automated quantitative gait analysis as a novel method to assess mechanical allodynia in the rat; a comparison with von Frey testing. Pain. 2003;102:203–9.CrossRefPubMed
8.
go back to reference Khan N, Smith MT. Multiple sclerosis-induced neuropathic pain: pharmacological management and pathophysiological insights from rodent EAE models. Inflammopharmacology. 2014;22:1–22.CrossRefPubMed Khan N, Smith MT. Multiple sclerosis-induced neuropathic pain: pharmacological management and pathophysiological insights from rodent EAE models. Inflammopharmacology. 2014;22:1–22.CrossRefPubMed
9.
go back to reference Lühder F, Gold R, Flügel A, Linker RA. Brain-derived neurotrophic factor in neuroimmunology: lessons learned from multiple sclerosis patients and experimental autoimmune encephalomyelitis models. Arch Immunol Ther Exp. 2013; 61:95–105. Lühder F, Gold R, Flügel A, Linker RA. Brain-derived neurotrophic factor in neuroimmunology: lessons learned from multiple sclerosis patients and experimental autoimmune encephalomyelitis models. Arch Immunol Ther Exp. 2013; 61:95–105.
10.
go back to reference Lassmann H, Bradl M. Multiple sclerosis: experimental models and reality. Acta Neuropathol. 2017;133(2):223–44.CrossRefPubMed Lassmann H, Bradl M. Multiple sclerosis: experimental models and reality. Acta Neuropathol. 2017;133(2):223–44.CrossRefPubMed
11.
go back to reference Recks MS, Addicks K, Kuerten S. Spinal cord histopathology of MOG peptide 35-55-induced experimental autoimmune encephalomyelitis is time- and score-dependent. Neurosci Lett. 2011;494:227–31.CrossRefPubMed Recks MS, Addicks K, Kuerten S. Spinal cord histopathology of MOG peptide 35-55-induced experimental autoimmune encephalomyelitis is time- and score-dependent. Neurosci Lett. 2011;494:227–31.CrossRefPubMed
12.
go back to reference Fiander MDJ, Stifani N, Nichols M, Akay T, Robertson GS. Kinematic gait parameters are highly sensitive measures of motor deficits and spinal cord injury in mice subjected to experimental autoimmune encephalomyelitis. Behav Brain Res. 2017;317:95–108.CrossRefPubMed Fiander MDJ, Stifani N, Nichols M, Akay T, Robertson GS. Kinematic gait parameters are highly sensitive measures of motor deficits and spinal cord injury in mice subjected to experimental autoimmune encephalomyelitis. Behav Brain Res. 2017;317:95–108.CrossRefPubMed
13.
go back to reference Rodrigues DH, Sachs D, Teixeira AL. Mechanical hypernociception in experimental autoimmune encephalomyelitis. Arq Neuropsiquiatr. 2009;67:78–81.CrossRefPubMed Rodrigues DH, Sachs D, Teixeira AL. Mechanical hypernociception in experimental autoimmune encephalomyelitis. Arq Neuropsiquiatr. 2009;67:78–81.CrossRefPubMed
14.
go back to reference Rodrigues DH, Leles BP, Costa VV, Miranda AS, Cisalpino D, Gomes DA, et al. IL-1b is involved with the generation of pain in experimental autoimmune encephalomyelitis. Mol Neurobiol. 2016;53:6540–7.CrossRefPubMed Rodrigues DH, Leles BP, Costa VV, Miranda AS, Cisalpino D, Gomes DA, et al. IL-1b is involved with the generation of pain in experimental autoimmune encephalomyelitis. Mol Neurobiol. 2016;53:6540–7.CrossRefPubMed
15.
go back to reference Chen Y-J, Cheng F-C, Sheu M-L, Su H-L, Chen C-J, Sheehan J, et al. Detection of subtle neurological alterations by the catwalk XT gait analysis system. J Neuroeng Rehabil. 2014;11:62.CrossRefPubMedPubMedCentral Chen Y-J, Cheng F-C, Sheu M-L, Su H-L, Chen C-J, Sheehan J, et al. Detection of subtle neurological alterations by the catwalk XT gait analysis system. J Neuroeng Rehabil. 2014;11:62.CrossRefPubMedPubMedCentral
16.
go back to reference Gabriel AF, Marcus MAE, Honig WMM, Walenkamp GHIM, Joosten EAJ. The CatWalk method: a detailed analysis of behavioral changes after acute inflammatory pain in the rat. J Neurosci Methods. 2007;163:9–16.CrossRefPubMed Gabriel AF, Marcus MAE, Honig WMM, Walenkamp GHIM, Joosten EAJ. The CatWalk method: a detailed analysis of behavioral changes after acute inflammatory pain in the rat. J Neurosci Methods. 2007;163:9–16.CrossRefPubMed
17.
go back to reference Pitzer C, Kuner R, Tappe-theodor A. Voluntary and evoked behavioral correlates in inflammatory pain conditions under different social housing conditions. Mol Pain. 2016;12:1–15.CrossRef Pitzer C, Kuner R, Tappe-theodor A. Voluntary and evoked behavioral correlates in inflammatory pain conditions under different social housing conditions. Mol Pain. 2016;12:1–15.CrossRef
18.
go back to reference Silva GAA, Pradella F, Moraes A, Farias A, dos Santos LMB, de Oliveira ALR, et al. Impact of pregabalin treatment on synaptic plasticity and glial reactivity during the course of experimental autoimmune encephalomyelitis. Brain Behav. 2014;4:925–35.CrossRefPubMedPubMedCentral Silva GAA, Pradella F, Moraes A, Farias A, dos Santos LMB, de Oliveira ALR, et al. Impact of pregabalin treatment on synaptic plasticity and glial reactivity during the course of experimental autoimmune encephalomyelitis. Brain Behav. 2014;4:925–35.CrossRefPubMedPubMedCentral
19.
go back to reference Herold S, Kumar P, Jung K, Graf I, Menkhoff H, Schulz X, et al. CatWalk gait analysis in a rat model of multiple sclerosis. BMC Neurosci. BioMed Central; 2016; 17:78. Herold S, Kumar P, Jung K, Graf I, Menkhoff H, Schulz X, et al. CatWalk gait analysis in a rat model of multiple sclerosis. BMC Neurosci. BioMed Central; 2016; 17:78.
20.
go back to reference Basso DM, Hansen CN. Biological basis of exercise-based treatments: spinal cord injury. Phys Med Rehabil. 2011;3:S73–7. Basso DM, Hansen CN. Biological basis of exercise-based treatments: spinal cord injury. Phys Med Rehabil. 2011;3:S73–7.
21.
go back to reference Pearson M, Dieberg G, Smart N. Exercise as a therapy for improvement of walking ability in adults with multiple sclerosis: a meta-analysis. Arch Phys Med Rehabil. 2015;96:1339–48.CrossRefPubMed Pearson M, Dieberg G, Smart N. Exercise as a therapy for improvement of walking ability in adults with multiple sclerosis: a meta-analysis. Arch Phys Med Rehabil. 2015;96:1339–48.CrossRefPubMed
22.
go back to reference Jung SY, Kim DY, Yune TY, Shin DH, Baek S Bin, Kim CJ. Treadmill exercise reduces spinal cord injury-induced apoptosis by activating the PI3K/Akt pathway in rats. Exp Ther Med. 2014; 7:587–93. Jung SY, Kim DY, Yune TY, Shin DH, Baek S Bin, Kim CJ. Treadmill exercise reduces spinal cord injury-induced apoptosis by activating the PI3K/Akt pathway in rats. Exp Ther Med. 2014; 7:587–93.
23.
go back to reference Rossi S, Furlan R, De Chiara V, Musella A, Lo Giudice T, Mataluni G, et al. Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol Dis. 2009;36:51–9.CrossRefPubMed Rossi S, Furlan R, De Chiara V, Musella A, Lo Giudice T, Mataluni G, et al. Exercise attenuates the clinical, synaptic and dendritic abnormalities of experimental autoimmune encephalomyelitis. Neurobiol Dis. 2009;36:51–9.CrossRefPubMed
24.
go back to reference Bernardes D, Brambilla R, Bracchi-Ricard V, Karmally S, Dellarole A, Carvalho-Tavares J, et al. Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis. J Neurochem. 2016;136:63–73.CrossRefPubMed Bernardes D, Brambilla R, Bracchi-Ricard V, Karmally S, Dellarole A, Carvalho-Tavares J, et al. Prior regular exercise improves clinical outcome and reduces demyelination and axonal injury in experimental autoimmune encephalomyelitis. J Neurochem. 2016;136:63–73.CrossRefPubMed
25.
go back to reference Bernardes D, Oliveira-Lima OC, da Silva TV, Faraco CCF, Leite HR, Juliano MA, et al. Differential brain and spinal cord cytokine and BDNF levels in experimental autoimmune encephalomyelitis are modulated by prior and regular exercise. J Neuroimmunol. 2013;264:24–34.CrossRefPubMed Bernardes D, Oliveira-Lima OC, da Silva TV, Faraco CCF, Leite HR, Juliano MA, et al. Differential brain and spinal cord cytokine and BDNF levels in experimental autoimmune encephalomyelitis are modulated by prior and regular exercise. J Neuroimmunol. 2013;264:24–34.CrossRefPubMed
26.
go back to reference Bernardes D, Oliveira-Lima OC, da Silva TV, Juliano MA, Dos Santos DM, Carvalho-Tavares J. Metabolic alterations in experimental autoimmune encephalomyelitis in mice: effects of prior physical exercise. Neurophysiology. 2016;48:117–21.CrossRef Bernardes D, Oliveira-Lima OC, da Silva TV, Juliano MA, Dos Santos DM, Carvalho-Tavares J. Metabolic alterations in experimental autoimmune encephalomyelitis in mice: effects of prior physical exercise. Neurophysiology. 2016;48:117–21.CrossRef
27.
go back to reference Le Page C, Ferry A, Rieu M. Effect of muscular exercise on chronic relapsing experimental autoimmune encephalomyelitis. J Appl Physiol. 1994;77(5):2341–7.PubMed Le Page C, Ferry A, Rieu M. Effect of muscular exercise on chronic relapsing experimental autoimmune encephalomyelitis. J Appl Physiol. 1994;77(5):2341–7.PubMed
28.
go back to reference Le Page C, Bourdoulous S, Béraud E, Couraud PO, Rieu M, Ferry A. Effect of physical exercise on adoptive experimental auto-immune encephalomyelitis in rats. Eur J Appl Occup Physiol. 1996;73(1-2):130–5.CrossRef Le Page C, Bourdoulous S, Béraud E, Couraud PO, Rieu M, Ferry A. Effect of physical exercise on adoptive experimental auto-immune encephalomyelitis in rats. Eur J Appl Occup Physiol. 1996;73(1-2):130–5.CrossRef
29.
go back to reference Patel DI, White LJ. Effect of 10-day forced treadmill training on neurotrophic factors in experimental autoimmune encephalomyelitis. Appl Physiol Nutr Metab. 2013;38:194–9.CrossRefPubMed Patel DI, White LJ. Effect of 10-day forced treadmill training on neurotrophic factors in experimental autoimmune encephalomyelitis. Appl Physiol Nutr Metab. 2013;38:194–9.CrossRefPubMed
30.
go back to reference Wens I, Dalgas U, Verboven K, Kosten L, Stevens A, Hens N, et al. Impact of high intensity exercise on muscle morphology in EAE rats. Physiol Res. 2015;32:1–37. Wens I, Dalgas U, Verboven K, Kosten L, Stevens A, Hens N, et al. Impact of high intensity exercise on muscle morphology in EAE rats. Physiol Res. 2015;32:1–37.
31.
go back to reference Patel DI, White LJ, Lira VA, Criswell DS, Physiology A. Forced exercise increases muscle mass in EAE despite early onset of disability. Physiol Res. 2016;65:1013–7.PubMed Patel DI, White LJ, Lira VA, Criswell DS, Physiology A. Forced exercise increases muscle mass in EAE despite early onset of disability. Physiol Res. 2016;65:1013–7.PubMed
32.
go back to reference 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;2013:1–12.CrossRef 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;2013:1–12.CrossRef
33.
go back to reference Bárez-López S, Bosch-García D, Gómez-Andrés D, Pulido-Valdeolivas I, Montero-Pedrazuela A, Obregon MJ, et al. Abnormal motor phenotype at adult stages in mice lacking type 2 deiodinase. PLoS One. 2014;9:e103857.CrossRefPubMedPubMedCentral Bárez-López S, Bosch-García D, Gómez-Andrés D, Pulido-Valdeolivas I, Montero-Pedrazuela A, Obregon MJ, et al. Abnormal motor phenotype at adult stages in mice lacking type 2 deiodinase. PLoS One. 2014;9:e103857.CrossRefPubMedPubMedCentral
34.
go back to reference de Haas R, Russel FG, Smeitink JA. Gait analysis in a mouse model resembling Leigh disease. Behav Brain Res. 2016;296:191–8.CrossRefPubMed de Haas R, Russel FG, Smeitink JA. Gait analysis in a mouse model resembling Leigh disease. Behav Brain Res. 2016;296:191–8.CrossRefPubMed
35.
go back to reference Wooley CM, Xing S, Burgess RW, Cox GA, Seburn KL. Age, experience and genetic background influence treadmill walking in mice. Physiol Behav. 2009;96:350–61.CrossRefPubMed Wooley CM, Xing S, Burgess RW, Cox GA, Seburn KL. Age, experience and genetic background influence treadmill walking in mice. Physiol Behav. 2009;96:350–61.CrossRefPubMed
36.
go back to reference Contarteze RVL, Manchado FDB, Gobatto CA, De Mello MAR. Stress biomarkers in rats submitted to swimming and treadmill running exercises. Comp Biochem Physiol - A Mol Integr Physiol. 2008;151:415–22.CrossRefPubMed Contarteze RVL, Manchado FDB, Gobatto CA, De Mello MAR. Stress biomarkers in rats submitted to swimming and treadmill running exercises. Comp Biochem Physiol - A Mol Integr Physiol. 2008;151:415–22.CrossRefPubMed
37.
go back to reference Baptista S, Piloto N, Reis F, Teixeira-de-Lemos E, Garrido AP, Dias A, et al. Treadmill running and swimming imposes distinct cardiovascular physiological adaptations in the rat: focus on serotonergic and sympathetic nervous systems modulation. Acta Physiol Hung. 2008;95:365–81.CrossRefPubMed Baptista S, Piloto N, Reis F, Teixeira-de-Lemos E, Garrido AP, Dias A, et al. Treadmill running and swimming imposes distinct cardiovascular physiological adaptations in the rat: focus on serotonergic and sympathetic nervous systems modulation. Acta Physiol Hung. 2008;95:365–81.CrossRefPubMed
38.
go back to reference Ra S-M, Kim H, Jang M-H, Shin M-C, Shin M-C, Lee T-H, et al. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci Lett. 2002;333:123–6.CrossRefPubMed Ra S-M, Kim H, Jang M-H, Shin M-C, Shin M-C, Lee T-H, et al. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci Lett. 2002;333:123–6.CrossRefPubMed
39.
go back to reference Deforges S, Branchu J, Biondi O, Grondard C, Pariset C, Lécolle S, et al. Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis. J Physiol. 2009;587:3561–72.CrossRefPubMedPubMedCentral Deforges S, Branchu J, Biondi O, Grondard C, Pariset C, Lécolle S, et al. Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis. J Physiol. 2009;587:3561–72.CrossRefPubMedPubMedCentral
40.
go back to reference Sheridan GK, Dev KK. Targeting S1P receptors in experimental autoimmune encephalomyelitis in mice improves early deficits in locomotor activity and increases ultrasonic vocalisations. Sci Rep. 2014;4:1–6. Sheridan GK, Dev KK. Targeting S1P receptors in experimental autoimmune encephalomyelitis in mice improves early deficits in locomotor activity and increases ultrasonic vocalisations. Sci Rep. 2014;4:1–6.
41.
go back to reference Deumens R, Jaken RJP, Marcus MAE, Joosten EAJ. The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J Neurosci Methods. 2007;164:120–30.CrossRefPubMed Deumens R, Jaken RJP, Marcus MAE, Joosten EAJ. The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J Neurosci Methods. 2007;164:120–30.CrossRefPubMed
42.
go back to reference Herbin M, Hackert R, Gasc JP, Renous S. Gait parameters of treadmill versus overground locomotion in mouse. Behav Brain Res. 2007;181:173–9.CrossRefPubMed Herbin M, Hackert R, Gasc JP, Renous S. Gait parameters of treadmill versus overground locomotion in mouse. Behav Brain Res. 2007;181:173–9.CrossRefPubMed
43.
go back to reference Batka RJ, Brown TJ, Mcmillan KP, Meadows RM, Jones KJ, Haulcomb MM. The need for speed in rodent locomotion analyses Richard. Anat Rec. 2014;297:1839–64.CrossRef Batka RJ, Brown TJ, Mcmillan KP, Meadows RM, Jones KJ, Haulcomb MM. The need for speed in rodent locomotion analyses Richard. Anat Rec. 2014;297:1839–64.CrossRef
44.
go back to reference Górska T, Majczyński H, Zmysłowski W. Overground locomotion in intact rats: contact electrode recording. Acta Neurobiol Exp (Wars). 1998;58:227–37. Górska T, Majczyński H, Zmysłowski W. Overground locomotion in intact rats: contact electrode recording. Acta Neurobiol Exp (Wars). 1998;58:227–37.
46.
go back to reference Moore S, Khalaj AJ, Patel R, Yoon J, Ichwan D, Hayardeny L, et al. Restoration of axon conduction and motor deficits by therapeutic treatment with glatiramer acetate. J Neurosci Res. 2014;92:1621–36.CrossRefPubMedPubMedCentral Moore S, Khalaj AJ, Patel R, Yoon J, Ichwan D, Hayardeny L, et al. Restoration of axon conduction and motor deficits by therapeutic treatment with glatiramer acetate. J Neurosci Res. 2014;92:1621–36.CrossRefPubMedPubMedCentral
47.
go back to reference Mitra NK, Bindal U, Hwa WE, Chua CLL, Tan CY. Evaluation of locomotor function and microscopic structure of the spinal cord in a mouse model of experimental autoimmune encephalomyelitis following treatment with syngeneic mesenchymal stem cells. Int J Clin Exp Pathol. 2015;8:12041–52.PubMedPubMedCentral Mitra NK, Bindal U, Hwa WE, Chua CLL, Tan CY. Evaluation of locomotor function and microscopic structure of the spinal cord in a mouse model of experimental autoimmune encephalomyelitis following treatment with syngeneic mesenchymal stem cells. Int J Clin Exp Pathol. 2015;8:12041–52.PubMedPubMedCentral
48.
go back to reference Starkey ML, Barritt AW, Yip PK, Davies M, Hamers FPT, McMahon SB, et al. Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp Neurol. 2005;195:524–39.CrossRefPubMed Starkey ML, Barritt AW, Yip PK, Davies M, Hamers FPT, McMahon SB, et al. Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp Neurol. 2005;195:524–39.CrossRefPubMed
49.
go back to reference Guillot TS, Asress SA, Richardson JR, Glass JD, Miller GW. Treadmill gait analysis does not detect motor deficits in animal models of Parkinson’s disease or amyotrophic lateral sclerosis. J Mot Behav. 2008;40:568–77.CrossRefPubMedPubMedCentral Guillot TS, Asress SA, Richardson JR, Glass JD, Miller GW. Treadmill gait analysis does not detect motor deficits in animal models of Parkinson’s disease or amyotrophic lateral sclerosis. J Mot Behav. 2008;40:568–77.CrossRefPubMedPubMedCentral
50.
go back to reference Liu Z, Li Y, Zhang J, Elias S, Chopp M. Evaluation of corticospinal axon loss by fluorescent dye tracing in mice with experimental autoimmune encephalomyelitis. J Neurosci Methods. 2008;167:191–7.CrossRefPubMed Liu Z, Li Y, Zhang J, Elias S, Chopp M. Evaluation of corticospinal axon loss by fluorescent dye tracing in mice with experimental autoimmune encephalomyelitis. J Neurosci Methods. 2008;167:191–7.CrossRefPubMed
51.
go back to reference Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, et al. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci. 2009;29:3442–52.CrossRefPubMed Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, et al. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci. 2009;29:3442–52.CrossRefPubMed
52.
go back to reference Gentile A, Fresegna D, Federici M, Musella A, Rizzo FR, Sepman H, et al. Dopaminergic dysfunction is associated with IL-1b-dependent mood alterations in experimental autoimmune encephalomyelitis. Neurobiol Dis. 2015;74:347–58.CrossRefPubMed Gentile A, Fresegna D, Federici M, Musella A, Rizzo FR, Sepman H, et al. Dopaminergic dysfunction is associated with IL-1b-dependent mood alterations in experimental autoimmune encephalomyelitis. Neurobiol Dis. 2015;74:347–58.CrossRefPubMed
53.
go back to reference Serradj N, Jamon M. The adaptation of limb kinematics to increasing walking speeds in freely moving mice 129/Sv and C57BL/6. Behav Brain Res. 2009;201:59–65.CrossRefPubMed Serradj N, Jamon M. The adaptation of limb kinematics to increasing walking speeds in freely moving mice 129/Sv and C57BL/6. Behav Brain Res. 2009;201:59–65.CrossRefPubMed
54.
go back to reference Koblinger K, Füzesi T, Ejdrygiewicz J, Krajacic A, Bains JS, Whelan PJ. Characterization of A11 neurons projecting to the spinal cord of mice. PLoS One. 2014;9:1–12.CrossRef Koblinger K, Füzesi T, Ejdrygiewicz J, Krajacic A, Bains JS, Whelan PJ. Characterization of A11 neurons projecting to the spinal cord of mice. PLoS One. 2014;9:1–12.CrossRef
Metadata
Title
Comprehensive catwalk gait analysis in a chronic model of multiple sclerosis subjected to treadmill exercise training
Authors
Danielle Bernardes
Alexandre Leite Rodrigues Oliveira
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2017
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-017-0941-z

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