Rehabilitation following spinal cord injury:how animal models can help our understanding of exercise-induced neuroplasticity
详细信息    查看全文 | 推荐本文 |
  • 英文篇名:Rehabilitation following spinal cord injury:how animal models can help our understanding of exercise-induced neuroplasticity
  • 作者:Kristina ; Loy ; Florence ; M.Bareyre
  • 英文作者:Kristina Loy;Florence M.Bareyre;Institute of Clinical Neuroimmunology, Ludwig-Maximilians Universit?t München;Munich Cluster of Systems Neurology (SyNergy);
  • 英文关键词:remodeling;;exercise;;wheel running;;treadmill;;detour circuit;;propriospinal neuron;;corticospinal tract;;raphespinal tract;;reticulospinal tract;;activity;;recovery;;central nervous system
  • 中文刊名:SJZY
  • 英文刊名:中国神经再生研究(英文版)
  • 机构:Institute of Clinical Neuroimmunology, Ludwig-Maximilians Universit?t München;Munich Cluster of Systems Neurology (SyNergy);
  • 出版日期:2018-12-28
  • 出版单位:Neural Regeneration Research
  • 年:2019
  • 期:v.14
  • 基金:Work in FMB laboratory is supported by grants from the Deutsche Forschungsgemeinschaft(DFG,SFB870);; by the Munich Center for Neurosciences(MCN);; the Wings for Life foundation;; supported by the Munich Center for Systems Neurology(DFG,SyNergy;EXC 1010)
  • 语种:英文;
  • 页:SJZY201903007
  • 页数:8
  • CN:03
  • ISSN:11-5422/R
  • 分类号:39-46
摘要
Spinal cord injury is a devastating condition that is followed by long and often unsuccessful recovery after trauma. The state of the art approach to manage paralysis and concomitant impairments is rehabilitation, which is the only strategy that has proven to be effective and beneficial for the patients over the last decades. How rehabilitation influences the remodeling of spinal axonal connections in patients is important to understand, in order to better target these changes and define the optimal timing and onset of training. While clinically the answers to these questions remain difficult to obtain, rodent models of rehabilitation like bicycling, treadmill training, swimming, enriched environments or wheel running that mimic clinical rehabilitation can be helpful to reveal the axonal changes underlying motor recovery. This review will focus on the different animal models of spinal cord injury rehabilitation and the underlying changes in neuronal networks that are improved by exercise and rehabilitation.
        Spinal cord injury is a devastating condition that is followed by long and often unsuccessful recovery after trauma. The state of the art approach to manage paralysis and concomitant impairments is rehabilitation, which is the only strategy that has proven to be effective and beneficial for the patients over the last decades. How rehabilitation influences the remodeling of spinal axonal connections in patients is important to understand, in order to better target these changes and define the optimal timing and onset of training. While clinically the answers to these questions remain difficult to obtain, rodent models of rehabilitation like bicycling, treadmill training, swimming, enriched environments or wheel running that mimic clinical rehabilitation can be helpful to reveal the axonal changes underlying motor recovery. This review will focus on the different animal models of spinal cord injury rehabilitation and the underlying changes in neuronal networks that are improved by exercise and rehabilitation.
引文
Abbott A(2014)Biomedicine:the changing face of primate research.Nature 506:24-26.
    Anderson KD,Guest JD,Dietrich WD,Bartlett Bunge M,Curiel R,Dididze M,Green BA,Khan A,Pearse DD,Saraf-Lavi E,Widerstrom-Noga E,Wood P,Levi AD(2017)Safety of autologous human schwann cell transplantation in subacute thoracic spinal cord injury.J Neurotrauma 34:2950-2963.
    Angeli CA,Boakye M,Morton RA,Vogt J,Benton K,Chen Y,Ferreira CK,Harkema SJ(2018)Recovery of over-ground walking after chronic motor complete spinal cord injury.N Engl J Med379:1244-1250.
    Armour BS,Courtney-Long EA,Fox MH,Fredine H,Cahill A(2016)Prevalence and causes of paralysis-United States,2013.Am J Public Health 106:1855-1857.
    Asboth L,Friedli L,Beauparlant J,Martinez-Gonzalez C,Anil S,Rey E,Baud L,Pidpruzhnykova G,Anderson MA,Shkorbatova P,Batti L,Pages S,Kreider J,Schneider BL,Barraud Q,Courtine G(2018)Cortico-reticulo-spinal circuit reorganization enables functional recovery after severe spinal cord contusion.Nat Neurosci 21:576-588.
    Baker SN(2011)The primate reticulospinal tract,hand function and functional recovery.J Physiol 589:5603-5612.
    Ballion B,Branchereau P,Chapron J,Viala D(2002)Ontogeny of descending serotonergic innervation and evidence for intraspinal 5-HT neurons in the mouse spinal cord.Brain Res Dev Brain Res 137:81-88.
    Bareyre FM,Kerschensteiner M,Raineteau O,Mettenleiter TC,Weinmann O,Schwab ME(2004)The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats.Nat Neurosci 7:269-277.
    Basso DM,Beattie MS,Bresnahan JC(1995)A sensitive and reliable locomotor rating scale for open field testing in rats.J Neurotrauma 12:1-21.
    Bose PK,Hou J,Parmer R,Reier PJ,Thompson FJ(2012)Altered patterns of reflex excitability,balance,and locomotion following spinal cord injury and locomotor training.Front Physiol 3:258.
    Bradbury EJ,Moon LD,Popat RJ,King VR,Bennett GS,Patel PN,Fawcett JW,McMahon SB(2002)Chondroitinase ABCpromotes functional recovery after spinal cord injury.Nature416:636-640.
    Brazg G,Fahey M,Holleran CL,Connolly M,Woodward J,Hennessy PW,Schmit BD,Hornby TG(2017)Effects of training intensity on locomotor performance in individuals with chronic spinal cord injury:a randomized crossover study.Neurorehabil Neural Repair 31:944-954.
    Brown DA,Johnson MS,Armstrong CJ,Lynch JM,Caruso NM,Ehlers LB,Fleshner M,Spencer RL,Moore RL(2007)Short-term treadmill running in the rat:what kind of stressor is it?J Appl Physiol(1985)103:1979-1985.
    Burns AS,Marino RJ,Kalsi-Ryan S,Middleton JW,Tetreault LA,Dettori JR,Mihalovich KE,Fehlings MG(2017)Type and timing of rehabilitation following acute and subacute spinal cord injury:a systematic review.Global Spine J 7:175s-194s.
    Bydon M,Lin J,Macki M,Gokaslan ZL,Bydon A(2014)The current role of steroids in acute spinal cord injury.World Neurosurg 82:848-854.
    Caudle KL,Brown EH,Shum-Siu A,Burke DA,Magnuson TS,Voor MJ,Magnuson DS(2011)Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat.Neurorehabil Neural Repair 25:729-739.
    Cetinkaya C,Sisman AR,Kiray M,Camsari UM,Gencoglu C,Baykara B,Aksu I,Uysal N(2013)Positive effects of aerobic exercise on learning and memory functioning,which correlate with hippocampal IGF-1 increase in adolescent rats.Neurosci Lett549:177-181.
    Chen K,Marsh BC,Cowan M,Al’Joboori YD,Gigout S,Smith CC,Messenger N,Gamper N,Schwab ME,Ichiyama RM(2017)Sequential therapy of anti-Nogo-A antibody treatment and treadmill training leads to cumulative improvements after spinal cord injury in rats.Exp Neurol 292:135-144.
    Cheng MY,Wang EH,Woodson WJ,Wang S,Sun G,Lee AG,Arac A,Fenno LE,Deisseroth K,Steinberg GK(2014)Optogenetic neuronal stimulation promotes functional recovery after stroke.Proc Natl Acad Sci U S A 111:12913-12918.
    Cote MP,Murray M,Lemay MA(2017)Rehabilitation strategies after spinal cord injury:inquiry into the mechanisms of success and failure.J Neurotrauma 34:1841-1857.
    Curt A,Levi AD,Schwab JM(2017)Challenges to translation and the hippocratic oath by premature termination of spinal cord stem cell-based trials.JAMA Neurol 74:635-636.
    Engesser-Cesar C,Anderson AJ,Basso DM,Edgerton VR,Cotman CW(2005)Voluntary wheel running improves recovery from a moderate spinal cord injury.J Neurotrauma 22:157-171.
    Engesser-Cesar C,Ichiyama RM,Nefas AL,Hill MA,Edgerton VR,Cotman CW,Anderson AJ(2007)Wheel running following spinal cord injury improves locomotor recovery and stimulates serotonergic fiber growth.Eur J Neurosci 25:1931-1939.
    Erschbamer MK,Pham TM,Zwart MC,Baumans V,Olson L(2006)Neither environmental enrichment nor voluntary wheel running enhances recovery from incomplete spinal cord injury in rats.Exp Neurol 201:154-164.
    Filli L,Engmann AK,Zorner B,Weinmann O,Moraitis T,Gullo M,Kasper H,Schneider R,Schwab ME(2014)Bridging the gap:a reticulo-propriospinal detour bypassing an incomplete spinal cord injury.J Neurosci 34:13399-13410.
    Fisahn C,Aach M,Jansen O,Moisi M,Mayadev A,Pagarigan KT,Dettori JR,Schildhauer TA(2016)The effectiveness and safety of exoskeletons as assistive and rehabilitation devices in the treatment of neurologic gait disorders in patients with spinal cord injury:a systematic review.Global Spine J 6:822-841.
    Fong AJ,Cai LL,Otoshi CK,Reinkensmeyer DJ,Burdick JW,Roy RR,Edgerton VR(2005)Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training.JNeurosci 25:11738-11747.
    Friedli L,Rosenzweig ES,Barraud Q,Schubert M,Dominici N,Awai L,Nielson JL,Musienko P,Nout-Lomas Y,Zhong H,Zdunowski S,Roy RR,Strand SC,van den Brand R,Havton LA,Beattie MS,Bresnahan JC,Bezard E,Bloch J,Edgerton VR,et al.(2015)Pronounced species divergence in corticospinal tract reorganization and functional recovery after lateralized spinal cord injury favors primates.Sci Transl Med 7:302ra134.
    Garcia-Alias G,Barkhuysen S,Buckle M,Fawcett JW(2009)Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation.Nat Neurosci 12:1145-1151.
    Gerasimenko Y,Gorodnichev R,Moshonkina T,Sayenko D,Gad P,Reggie Edgerton V(2015)Transcutaneous electrical spinal-cord stimulation in humans.Ann Phys Rehabil Med 58:225-231.
    Gill ML,Grahn PJ,Calvert JS,Linde MB,Lavrov IA,Strommen JA,Beck LA,Sayenko DG,Van Straaten MG,Drubach DI,Veith DD,Thoreson AR,Lopez C,Gerasimenko YP,Edgerton VR,Lee KH,Zhao KD(2018)Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia.Nat Med doi:10.1038/s41591-018-0175-7.
    Gomes-Osman J,Cortes M,Guest J,Pascual-Leone A(2016)Asystematic review of experimental strategies aimed at improving motor function after acute and chronic spinal cord injury.J Neurotrauma 33:425-438.
    Gomez-Pinilla F,Ying Z,Opazo P,Roy RR,Edgerton VR(2001)Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle.Eur J Neurosci 13:1078-1084.
    Griesbach GS,Hovda DA,Molteni R,Wu A,Gomez-Pinilla F(2004)Voluntary exercise following traumatic brain injury:brain-derived neurotrophic factor upregulation and recovery of function.Neuroscience 125:129-139.
    Han Z,Lat I,Pollard SR(2014)Safety and efficacy of corticosteroid use in neurologic trauma.J Pharm Pract 27:487-495.
    Harkema SJ,Schmidt-Read M,Lorenz DJ,Edgerton VR,Behrman AL(2012)Balance and ambulation improvements in individuals with chronic incomplete spinal cord injury using locomotor training-based rehabilitation.Arch Phys Med Rehabil 93:1508-1517.
    Hashimoto T,Fukuda N(1991)Contribution of serotonin neurons to the functional recovery after spinal cord injury in rats.Brain Res 539:263-270.
    Hayashibe M,Homma T,Fujimoto K,Oi T,Yagi N,Kashihara M,Nishikawa N,Ishizumi Y,Abe S,Hashimoto H,Kanekiyo K,Imagita H,Ide C,Morioka S(2016)Locomotor improvement of spinal cord-injured rats through treadmill training by forced plantar placement of hind paws.Spinal Cord 54:521-529.
    Ilha J,Centenaro LA,Broetto Cunha N,de Souza DF,Jaeger M,do Nascimento PS,Kolling J,Ben J,Marcuzzo S,Wyse AT,Gottfried C,Achaval M(2011)The beneficial effects of treadmill step training on activity-dependent synaptic and cellular plasticity markers after complete spinal cord injury.Neurochem Res36:1046-1055.
    Jacobi A,Loy K,Schmalz AM,Hellsten M,Umemori H,Kerschensteiner M,Bareyre FM(2015)FGF22 signaling regulates synapse formation during post-injury remodeling of the spinal cord.The EMBO J 34:1231-1243.
    Jung SY,Seo TB,Kim DY(2016)Treadmill exercise facilitates recovery of locomotor function through axonal regeneration following spinal cord injury in rats.J Exerc Rehabil 12:284-292.
    Kakulas BA(2004)Neuropathology:the foundation for new treatments in spinal cord injury.Spinal Cord 42:549-563.
    Ke Z,Yip SP,Li L,Zheng XX,Tong KY(2011)The effects of voluntary,involuntary,and forced exercises on brain-derived neurotrophic factor and motor function recovery:a rat brain ischemia model.PLoS One 6:e16643.
    Lang C,Guo X,Kerschensteiner M,Bareyre FM(2012)Single collateral reconstructions reveal distinct phases of corticospinal remodeling after spinal cord injury.PLoS One 7:e30461.
    Lang C,Bradley PM,Jacobi A,Kerschensteiner M,Bareyre FM(2013)STAT3 promotes corticospinal remodelling and functional recovery after spinal cord injury.EMBO Rep 14:931-937.
    Lankhorst AJ,ter Laak MP,van Laar TJ,van Meeteren NL,de Groot JC,Schrama LH,Hamers FP,Gispen WH(2001)Effects of enriched housing on functional recovery after spinal cord contusive injury in the adult rat.J Neurotrauma 18:203-215.
    Lawrence DG,Kuypers HG(1968a)The functional organization of the motor system in the monkey.II.The effects of lesions of the descending brain-stem pathways.Brain 91:15-36.
    Lawrence DG,Kuypers HG(1968b)The functional organization of the motor system in the monkey.I.The effects of bilateral pyramidal lesions.Brain 91:1-14.
    Leal G,Comprido D,Duarte CB(2014)BDNF-induced local protein synthesis and synaptic plasticity.Neuropharmacology 76 Pt C:639-656.
    Li X,Wu Q,Xie C,Wang C,Wang Q,Dong C,Fang L,Ding J,Wang T(2018)Blocking of BDNF-TrkB signaling inhibits the promotion effect of neurological function recovery after treadmill training in rats with spinal cord injury.Spinal Cord doi:10.1038/s41393-018-0173-0.
    Liang H,Watson C,Paxinos G(2016)Terminations of reticulospinal fibers originating from the gigantocellular reticular formation in the mouse spinal cord.Brain Struct Funct 221:1623-1633.
    Little JW,Harris RM,Lerner SJ(1991)Immobilization impairs recovery after spinal cord injury.Arch Phys Med Rehabil 72:408-412.
    Liu K,Lu Y,Lee JK,Samara R,Willenberg R,Sears-Kraxberger I,Tedeschi A,Park KK,Jin D,Cai B,Xu B,Connolly L,Steward O,Zheng B,He Z(2010)PTEN deletion enhances the regenerative ability of adult corticospinal neurons.Nat Neurosci 13:1075-1081.
    Lovely RG,Gregor RJ,Roy RR,Edgerton VR(1986)Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat.Exp Neurol 92:421-435.
    Lovely RG,Gregor RJ,Roy RR,Edgerton VR(1990)Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats.Brain Res 514:206-218.
    Loy K,Schmalz A,Hoche T,Jacobi A,Kreutzfeldt M,Merkler D,Bareyre FM(2018)Enhanced voluntary exercise improves functional recovery following spinal cord injury by impacting the local neuroglial injury response and supporting the rewiring of supraspinal circuits.J Neurotrauma doi:10.1089/neu.2017.5544.
    Magnuson DS,Smith RR,Brown EH,Enzmann G,Angeli C,Quesada PM,Burke D(2009)Swimming as a model of task-specific locomotor retraining after spinal cord injury in the rat.Neurorehabil Neural Repair 23:535-545.
    Maier IC,Baumann K,Thallmair M,Weinmann O,Scholl J,Schwab ME(2008)Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury.J Neurosci28:9386-9403.
    Martinez M,Delivet-Mongrain H,Rossignol S(2013)Treadmill training promotes spinal changes leading to locomotor recovery after partial spinal cord injury in cats.J Neurophysiol 109:2909-2922.
    Mehrholz J,Harvey LA,Thomas S,Elsner B(2017)Is body-weightsupported treadmill training or robotic-assisted gait training superior to overground gait training and other forms of physiotherapy in people with spinal cord injury?A systematic review.Spinal Cord 55:722-729.
    Meijer JH,Robbers Y(2014)Wheel running in the wild.Proc Biol Sci 281:20140210.
    Minassian K,McKay WB,Binder H,Hofstoetter US(2016)Targeting lumbar spinal neural circuitry by epidural stimulation to restore motor function after spinal cord injury.Neurotherapeutics13:284-294.
    Morrison SA,Lorenz D,Eskay CP,Forrest GF,Basso DM(2018)Longitudinal recovery and reduced costs after 120 sessions of locomotor training for motor incomplete spinal cord injury.Arch Phys Med Rehabil 99:555-562.
    Nagel SJ,Wilson S,Johnson MD,Machado A,Frizon L,Chardon MK,Reddy CG,Gillies GT,Howard MA(2017)Spinal cord stimulation for spasticity:historical approaches,current status,and future directions.Neuromodulation 20:307-321.
    Neeper SA,Gomez-Pinilla F,Choi J,Cotman CW(1996)Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain.Brain Res 726:49-56.
    Oh SK,Choi KH,Yoo JY,Kim DY,Kim SJ,Jeon SR(2016)A phase III clinical trial showing limited efficacy of autologous mesenchymal stem cell therapy for spinal cord injury.Neurosurgery78:436-447.
    Rejc E,Angeli CA,Atkinson D,Harkema SJ(2017)Motor recovery after activity-based training with spinal cord epidural stimulation in a chronic motor complete paraplegic.Sci Rep 7:13476.
    Robert AA,Al Jadid MS,Bin Afif S,Al Sowyed AA,Al-Mubarak S(2010)The effects of different rehabilitation strategies on the functional recovery of spinal cord injured rats:an experimental study.Spine 35:E1273-1277.
    Rossignol S,Bouyer L(2004)Adaptive mechanisms of spinal locomotion in cats.Integr Comp Biol 44:71-79.
    Ruschel J,Hellal F,Flynn KC,Dupraz S,Elliott DA,Tedeschi A,Bates M,Sliwinski C,Brook G,Dobrindt K,Peitz M,Brustle O,Norenberg MD,Blesch A,Weidner N,Bunge MB,Bixby JL,Bradke F(2015)Axonal regeneration.Systemic administration of epothilone B promotes axon regeneration after spinal cord injury.Science 348:347-352.
    Sawada M,Kato K,Kunieda T,Mikuni N,Miyamoto S,Onoe H,Isa T,Nishimura Y(2015)Function of the nucleus accumbens in motor control during recovery after spinal cord injury.Science350:98-101.
    Shah PK,Garcia-Alias G,Choe J,Gad P,Gerasimenko Y,Tillakaratne N,Zhong H,Roy RR,Edgerton VR(2013)Use of quadrupedal step training to re-engage spinal interneuronal networks and improve locomotor function after spinal cord injury.Brain 136:3362-3377.
    Smith RR,Brown EH,Shum-Siu A,Whelan A,Burke DA,Benton RL,Magnuson DS(2009)Swim training initiated acutely after spinal cord injury is ineffective and induces extravasation in and around the epicenter.J Neurotrauma 26:1017-1027.
    Sun T,Ye C,Wu J,Zhang Z,Cai Y,Yue F(2013)Treadmill step training promotes spinal cord neural plasticity after incomplete spinal cord injury.Neural Regen Res 8:2540-2547.
    Takeoka A,Vollenweider I,Courtine G,Arber S(2014)Muscle spindle feedback directs locomotor recovery and circuit reorganization after spinal cord injury.Cell 159:1626-1639.
    van den Brand R,Heutschi J,Barraud Q,DiGiovanna J,Bartholdi K,Huerlimann M,Friedli L,Vollenweider I,Moraud EM,Duis S,Dominici N,Micera S,Musienko P,Courtine G(2012)Restoring voluntary control of locomotion after paralyzing spinal cord injury.Science 336:1182-1185.
    Van Meeteren NL,Eggers R,Lankhorst AJ,Gispen WH,Hamers FP(2003)Locomotor recovery after spinal cord contusion injury in rats is improved by spontaneous exercise.J Neurotrauma20:1029-1037.
    Venezia AC,Guth LM,Sapp RM,Spangenburg EE,Roth SM(2016)Sex-dependent and independent effects of long-term voluntary wheel running on Bdnf mRNA and protein expression.Physiol Behav 156:8-15.
    Wang H,Liu NK,Zhang YP,Deng L,Lu QB,Shields CB,Walker MJ,Li J,Xu XM(2015)Treadmill training induced lumbar motoneuron dendritic plasticity and behavior recovery in adult rats after a thoracic contusive spinal cord injury.Exp Neurol271:368-378.
    Weidner N,Ner A,Salimi N,Tuszynski MH(2001)Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury.Proc Natl Acad Sci U S A 98:3513-3518.
    Wernig A,Nanassy A,Muller S(1998)Maintenance of locomotor abilities following Laufband(treadmill)therapy in para-and tetraplegic persons:follow-up studies.Spinal Cord 36:744-749.
    Wernig A,Muller S,Nanassy A,Cagol E(1995)Laufband therapy based on‘rules of spinal locomotion’is effective in spinal cord injured persons.Eur J Neurosci 7:823-829.
    Yin Y,Sun W,Li Z,Zhang B,Cui H,Deng L,Xie P,Xiang J,Zou J(2013)Effects of combining methylprednisolone with rolipram on functional recovery in adult rats following spinal cord injury.Neurochem Int 62:903-912.
    Zhu H,Poon W,Liu Y,Leung GK-K,Wong Y,Feng Y,Ng SCP,Tsang KS,Sun DTF,Yeung DK,Shen C,Niu F,Xu Z,Tan P,Tang S,Gao H,Cha Y,So KF,Fleischaker R,Sun D,et al.(2016)Phase I-II clinical trial assessing safety and efficacy of umbilical cord blood mononuclear cell transplant therapy of chronic complete spinal cord injury.Cell Transplant 25:1925-1943.
    Zorner B,Schwab ME(2010)Anti-Nogo on the go:from animal models to a clinical trial.Ann N Y Acad Sci 1198 Suppl 1:E22-34.
    Zorner B,Bachmann LC,Filli L,Kapitza S,Gullo M,Bolliger M,Starkey ML,Rothlisberger M,Gonzenbach RR,Schwab ME(2014)Chasing central nervous system plasticity:the brainstem’s contribution to locomotor recovery in rats with spinal cord injury.Brain 137:1716-1732.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700