Potentials and limitations of peripheral nerve injury models in rodents with particular reference to the femoral nerve

Ahlborn, 2007, One hour electrical stimulation accelerates functional recovery after femoral nerve repair, Exp. Neurol., 208, 137, 10.1016/j.expneurol.2007.08.005 Al-Majed, 2000, Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration, J. Neurosci., 20, 2602, 10.1523/JNEUROSCI.20-07-02602.2000 Angelov, 2007, Mechanical stimulation of paralyzed vibrissal muscles following facial nerve injury in adult rat promotes full recovery of whisking, Neurobiol. Dis., 26, 229, 10.1016/j.nbd.2006.12.016 Apostolova, 2006, Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice, J. Neurosci., 26, 7849, 10.1523/JNEUROSCI.1526-06.2006 Badke, 1989, Maturation of transmission in reinnervated mouse soleus muscle, Muscle Nerve, 12, 580, 10.1002/mus.880120709 Basso, 2004, Behavioral testing after spinal cord injury: congruities, complexities, and controversies, J. Neurotrauma, 21, 395, 10.1089/089771504323004548 Blinzinger, 1968, Displacement of synaptic terminals from regenerating motoneurons by microglial cells, Z. Zellforsch. Mikrosk. Anat., 85, 145, 10.1007/BF00325030 Bozkurt, 2008, CatWalk gait analysis in assessment of functional recovery after sciatic nerve injury, J. Neurosci. Methods, 173, 91, 10.1016/j.jneumeth.2008.05.020 Brushart, 1988, Preferential reinnervation of motor nerves by regenerating motor axons, J. Neurosci., 8, 1026, 10.1523/JNEUROSCI.08-03-01026.1988 Brushart, 1993, Motor axons preferentially reinnervate motor pathways, J. Neurosci., 13, 2730, 10.1523/JNEUROSCI.13-06-02730.1993 Brushart, 2002, Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron, J. Neurosci., 22, 6631, 10.1523/JNEUROSCI.22-15-06631.2002 Brushart, 1980, Alteration in connections between muscle and anterior horn motoneurons after peripheral nerve repair, Science, 208, 603, 10.1126/science.7367884 Brännström, 1999, Recovery of synapses in axotomized adult cat spinal motoneurons after reinnervation into muscle, Exp. Brain Res., 125, 19, 10.1007/s002210050653 Chen, 2010, The extracellular matrix glycoprotein tenascin-C is beneficial for spinal cord regeneration, Mol. Ther., 18, 1769, 10.1038/mt.2010.133 Chen, 2007, Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury, Brain, 130, 954, 10.1093/brain/awm049 Chen, 2007, Peripheral regeneration, Annu. Rev. Neurosci., 30, 209, 10.1146/annurev.neuro.30.051606.094337 Chipman, 2010, Neural cell adhesion molecule is required for stability of reinnervated neuromuscular junctions, Eur. J. Neurosci., 31, 238, 10.1111/j.1460-9568.2009.07049.x Dahlin, 2009, Chapter 28: future perspective in peripheral nerve reconstruction, Int. Rev. Neurobiol., 87, 507, 10.1016/S0074-7742(09)87028-1 de Medinaceli, 1982, An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks, Exp. Neurol., 77, 634, 10.1016/0014-4886(82)90234-5 de Ruiter, 2008, Misdirection of regenerating motor axons after nerve injury and repair in the rat sciatic nerve model, Exp. Neurol., 211, 339, 10.1016/j.expneurol.2007.12.023 Deumens, 2007, The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection, J. Neurosci. Methods, 164, 120, 10.1016/j.jneumeth.2007.04.009 Eaton, 2003, Common animal models for spasticity and pain, J. Rehabil. Res. Dev., 40, 41, 10.1682/JRRD.2003.08.0041 Eberhardt, 2006, BDNF/TrkB signaling regulates HNK-1 carbohydrate expression in regenerating motor nerves and promotes functional recovery after peripheral nerve repair, Exp. Neurol., 198, 500, 10.1016/j.expneurol.2005.12.018 Erzurumlu, 1979, Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat, J. Comp. Neurol., 188, 75, 10.1002/cne.901880107 Fawcett, 2009, Molecular control of brain plasticity and repair, Prog. Brain Res., 175, 501, 10.1016/S0079-6123(09)17534-9 Fey, 2010, A novel motion analysis approach reveals late recovery in C57BL/6 mice and deficits in NCAM-deficient mice after sciatic nerve crush, J. Neurotrauma, 27, 815, 10.1089/neu.2009.1217 Filipe, 2006, Effect of skin movement on the analysis of hindlimb kinematics during treadmill locomotion in rats, J. Neurosci. Methods, 153, 55, 10.1016/j.jneumeth.2005.10.006 Franchi, 2000, Changes in motor representation related to facial nerve damage and regeneration in adult rats, Exp. Brain Res., 135, 53, 10.1007/s002210000503 Franz, 2008, Intrinsic neuronal properties control selective targeting of regenerating motoneurons, Brain, 131, 1492, 10.1093/brain/awn039 Franz, 2005, Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons, J. Neurosci., 25, 2081, 10.1523/JNEUROSCI.4880-04.2005 Fu, 1997, The cellular and molecular basis of peripheral nerve regeneration, Mol. Neurobiol., 14, 67, 10.1007/BF02740621 Galtrey, 2007, Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair, Brain, 130, 926, 10.1093/brain/awl372 Guntinas-Lichius, 2005, Opposite impacts of tenascin-C and tenascin-R deficiency in mice on the functional outcome of facial nerve repair, Eur. J. Neurosci., 22, 2171, 10.1111/j.1460-9568.2005.04424.x Guntinas-Lichius, 2005, Factors limiting motor recovery after facial nerve transection in the rat: combined structural and functional analyses, Eur. J. Neurosci., 21, 391, 10.1111/j.1460-9568.2005.03877.x Guntinas-Lichius, 2007, Quality of life after facial nerve repair, Laryngoscope, 117, 421, 10.1097/MLG.0b013e31802d83df Guseva, 2009, Ablation of adhesion molecule L1 in mice favours Schwann cell proliferation and functional recovery after peripheral nerve injury, Brain, 132, 2180, 10.1093/brain/awp160 Haftel, 2005, Central suppression of regenerated proprioceptive afferents, J. Neurosci., 25, 4733, 10.1523/JNEUROSCI.4895-04.2005 Hamilton, 2011, Misdirection of regenerating axons and functional recovery following sciatic nerve injury in rats, J. Comp. Neurol., 519, 21, 10.1002/cne.22446 Herbison, 1981, Contractile properties of reinnervating skeletal muscle in the rat, Arch. Phys. Med. Rehabil., 62, 35 Hildebrand, 1985, Myelin sheath remodelling in regenerated rat sciatic nerve, Brain Res., 358, 163, 10.1016/0006-8993(85)90960-6 Höke, 2006, Mechanisms of disease: what factors limit the success of peripheral nerve regeneration in humans?, Nat. Clin. Pract. Neurol., 2, 448, 10.1038/ncpneuro0262 Ijkema-Paassen, 2002, Reinnervation of muscles after transection of the sciatic nerve in adult rats, Muscle Nerve, 25, 891, 10.1002/mus.10130 Irintchev, 1991, Effects on recovery of soleus and extensor digitorum longus muscles of prolonged wheel running during a period of repeated nerve damage, Neuroscience, 44, 515, 10.1016/0306-4522(91)90074-X Irintchev, 1990, Reinnervation and recovery of mouse soleus muscle after long-term denervation, Neuroscience, 39, 231, 10.1016/0306-4522(90)90236-W Irintchev, 2005, Impacts of lesion severity and tyrosine kinase receptor B deficiency on functional outcome of femoral nerve injury assessed by a novel single-frame motion analysis in mice, Eur. J. Neurosci., 22, 802, 10.1111/j.1460-9568.2005.04274.x Isokawa-Akesson, 1987, Difference in projections to the lateral and medial facial nucleus: anatomically separate pathways for rhythmical vibrissa movement in rats, Exp. Brain Res., 65, 385, 10.1007/BF00236312 Jakovcevski, 2007, Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury, J. Neurosci., 27, 7222, 10.1523/JNEUROSCI.0739-07.2007 Jaquet, 2001, Median, ulnar, and combined median-ulnar nerve injuries: functional outcome and return to productivity, J. Trauma, 51, 687, 10.1097/00005373-200110000-00011 Kanaya, 1996, Sciatic function index, nerve conduction tests, muscle contraction, and axon morphometry as indicators of regeneration, Plast. Reconstr. Surg., 98, 1264, 10.1097/00006534-199612000-00023 Kiryakova, 2010, Recovery of whisking function promoted by manual stimulation of the vibrissal muscles after facial nerve injury requires insulin-like growth factor 1 (IGF-1), Exp. Neurol., 222, 226, 10.1016/j.expneurol.2009.12.031 Kiryu-Seo, 2006, Unique anti-apoptotic activity of EAAC1 in injured motor neurons, EMBO J., 25, 3411, 10.1038/sj.emboj.7601225 Kiryu-Seo, 2005, Noxa is a critical mediator of p53-dependent motor neuron death after nerve injury in adult mouse, J. Neurosci., 25, 1442, 10.1523/JNEUROSCI.4041-04.2005 Kleene, 2004, Glycans and neural cell interactions, Nat. Rev. Neurosci., 5, 195, 10.1038/nrn1349 Kocsis, 1983, Long-term regenerated nerve fibres retain sensitivity to potassium channel blocking agents, Nature, 304, 640, 10.1038/304640a0 Koerber, 1989, Mismatches between peripheral receptor type and central projections after peripheral nerve regeneration, Neurosci. Lett., 99, 67, 10.1016/0304-3940(89)90266-8 Krarup, 2002, Factors that influence peripheral nerve regeneration: an electrophysiological study of the monkey median nerve, Ann. Neurol., 51, 69, 10.1002/ana.10054 Kreiger, 1981, Injuries to the upper extremity: patterns of occurrence, Clin. Plast. Surg., 8, 13, 10.1016/S0094-1298(20)30469-7 Lago, 2006, Correlation between target reinnervation and distribution of motor axons in the injured rat sciatic nerve, J. Neurotrauma, 23, 227, 10.1089/neu.2006.23.227 Lee, 2009, Better functional outcome of compression spinal cord injury in mice is associated with enhanced H-reflex responses, Exp. Neurol., 216, 365, 10.1016/j.expneurol.2008.12.009 Lee, 2000, Peripheral nerve injury and repair, J. Am. Acad. Orthop. Surg., 8, 243, 10.5435/00124635-200007000-00005 Lindsay, 2010, Daily facial stimulation to improve recovery after facial nerve repair in rats, Arch. Facial Plast. Surg., 12, 180, 10.1001/archfacial.2010.39 Lundborg, 2003, Richard P. Bunge memorial lecture. Nerve injury and repair – a challenge to the plastic brain, J. Peripher. Nerv. Syst., 8, 209, 10.1111/j.1085-9489.2003.03027.x Lundborg, 2007, Hand function after nerve repair, Acta Physiol. (Oxf.), 189, 207, 10.1111/j.1748-1716.2006.01653.x Madison, 1996, Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons, J. Neurosci., 16, 5698, 10.1523/JNEUROSCI.16-18-05698.1996 Madison, 2007, The specificity of motor neurone regeneration (preferential reinnervation), Acta Physiol. (Oxf.), 189, 201, 10.1111/j.1748-1716.2006.01657.x Madison, 2009, Schwann cell influence on motor neuron regeneration accuracy, Neuroscience, 163, 213, 10.1016/j.neuroscience.2009.05.073 Malin, 2009, The extracellular-matrix protein matrilin 2 participates in peripheral nerve regeneration, J. Cell Sci., 122, 995, 10.1242/jcs.040378 Martin, 2005, Adult motor neuron apoptosis is mediated by nitric oxide and Fas death receptor linked by DNA damage and p53 activation, J. Neurosci., 25, 6449, 10.1523/JNEUROSCI.0911-05.2005 Martini, 1986, Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve, J. Cell Biol., 103, 2439, 10.1083/jcb.103.6.2439 Martini, 1994, The L2/HNK-1 carbohydrate is preferentially expressed by previously motor axon-associated Schwann cells in reinnervated peripheral nerves, J. Neurosci., 14, 7180, 10.1523/JNEUROSCI.14-11-07180.1994 Martini, 1992, The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves, Eur. J. Neurosci., 4, 628, 10.1111/j.1460-9568.1992.tb00171.x Martins, 2006, Correlation between parameters of electrophysiological, histomorphometric and sciatic functional index evaluations after rat sciatic nerve repair, Arq. Neuropsiquiatr., 64, 750, 10.1590/S0004-282X2006000500010 McComas, 1998, Oro-facial muscles: internal structure, function and ageing, Gerodontology, 15, 3, 10.1111/j.1741-2358.1998.00003.x Mears, 2003, Antibodies to myelin-associated glycoprotein accelerate preferential motor reinnervation, J. Peripher. Nerv. Syst., 8, 91, 10.1046/j.1529-8027.2003.03012.x Mehanna, 2010, Polysialic acid glycomimetic promotes functional recovery and plasticity after spinal cord injury in mice, Mol. Ther., 18, 34, 10.1038/mt.2009.235 Mehanna, 2009, Polysialic acid glycomimetics promote myelination and functional recovery after peripheral nerve injury in mice, Brain, 132, 1449, 10.1093/brain/awp128 Mert, 2004, Role of potassium channels in the frequency-dependent activity of regenerating nerves, Pharmacology, 72, 157, 10.1159/000080100 Moran, 2004, The facial nerve axotomy model, Brain Res. Brain Res. Rev., 44, 154, 10.1016/j.brainresrev.2003.11.004 Muir, 2010, The potentiation of peripheral nerve sheaths in regeneration and repair, Exp. Neurol., 223, 102, 10.1016/j.expneurol.2009.05.038 Muir, 2000, Mini-review: assessment of behavioural recovery following spinal cord injury in rats, Eur. J. Neurosci., 12, 3079, 10.1046/j.1460-9568.2000.00205.x Munro, 1998, Lack of association between outcome measures of nerve regeneration, Muscle Nerve, 21, 1095, 10.1002/(SICI)1097-4598(199808)21:8<1095::AID-MUS20>3.0.CO;2-S Navarro, 2007, Neural plasticity after peripheral nerve injury and regeneration, Prog. Neurobiol., 82, 163, 10.1016/j.pneurobio.2007.06.005 Nguyen, 2005, Positive feedback in a brainstem tactile sensorimotor loop, Neuron, 45, 447, 10.1016/j.neuron.2004.12.042 Nichols, 2005, Choosing the correct functional assay: a comprehensive assessment of functional tests in the rat, Behav. Brain Res., 163, 143, 10.1016/j.bbr.2005.05.003 Noble, 1998, Analysis of upper and lower extremity peripheral nerve injuries in a population of patients with multiple injuries, J. Trauma, 45, 116, 10.1097/00005373-199807000-00025 Rice, 1997, Comprehensive immunofluorescence and lectin binding analysis of vibrissal follicle sinus complex innervation in the mystacial pad of the rat, J. Comp. Neurol., 385, 149, 10.1002/(SICI)1096-9861(19970825)385:2<149::AID-CNE1>3.0.CO;2-1 Robinson, 2003, Preferential motor reinnervation in the mouse: comparison of femoral nerve repair using a fibrin sealant or suture, Muscle Nerve, 28, 227, 10.1002/mus.10422 Robinson, 2004, Motor neurons can preferentially reinnervate cutaneous pathways, Exp. Neurol., 190, 407, 10.1016/j.expneurol.2004.08.007 Robinson, 2005, Manipulations of the mouse femoral nerve influence the accuracy of pathway reinnervation by motor neurons, Exp. Neurol., 192, 39, 10.1016/j.expneurol.2004.10.013 Robinson, 2006, Developmentally regulated changes in femoral nerve regeneration in the mouse and rat, Exp. Neurol., 197, 341, 10.1016/j.expneurol.2005.10.007 Robinson, 2000, Traumatic injury to peripheral nerves, Muscle Nerve, 23, 863, 10.1002/(SICI)1097-4598(200006)23:6<863::AID-MUS4>3.0.CO;2-0 Rutishauser, 2008, Polysialic acid in the plasticity of the developing and adult vertebrate nervous system, Nat. Rev. Neurosci., 9, 26, 10.1038/nrn2285 Sanes, 1990, Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions, Exp. Brain Res., 79, 479, 10.1007/BF00229318 Santos, 1995, Neuromuscular evaluation using rat gait analysis, J. Neurosci. Methods, 61, 79, 10.1016/0165-0270(95)00026-Q Schiaveto de Souza, 2004, Methodological evaluation to analyze functional recovery after sciatic nerve injury, J. Neurotrauma, 21, 627, 10.1089/089771504774129955 Scholz, 2009, Peripheral nerve injuries: an international survey of current treatments and future perspectives, J. Reconstr. Microsurg., 25, 339, 10.1055/s-0029-1215529 Shenaq, 1989, Reliability of sciatic function index in assessing nerve regeneration across a 1cm gap, Microsurgery, 10, 214, 10.1002/micr.1920100315 Siemionow, 2009, Chapter 8: current techniques and concepts in peripheral nerve repair, Int. Rev. Neurobiol., 87, 141, 10.1016/S0074-7742(09)87008-6 Simova, 2006, Carbohydrate mimics promote functional recovery after peripheral nerve repair, Ann. Neurol., 60, 430, 10.1002/ana.20948 Sinis, 2008, Manual stimulation of forearm muscles does not improve recovery of motor function after injury to a mixed peripheral nerve, Exp. Brain Res., 185, 469, 10.1007/s00221-007-1174-y Sumner, 1990, Aberrant reinnervation, Muscle Nerve, 13, 801, 10.1002/mus.880130905 Sunderland, 1991 Svensson, 1991, Synaptic detachment from hypoglossal neurons after different types of nerve injury in the cat, J. Hirnforsch., 32, 547 Taylor, 2009, Cutting your nerve changes your brain, Brain, 132, 3122, 10.1093/brain/awp231 Tomita, 2007, Myelin-associated glycoprotein reduces axonal branching and enhances functional recovery after sciatic nerve transection in rats, Glia, 55, 1498, 10.1002/glia.20566 Tomov, 2002, An example of neural plasticity evoked by putative behavioral demand and early use of vibrissal hairs after facial nerve transection, Exp. Neurol., 178, 207, 10.1006/exnr.2002.8040 Ugolini, 2003, Fas/tumor necrosis factor receptor death signaling is required for axotomy-induced death of motoneurons in vivo, J. Neurosci., 23, 8526, 10.1523/JNEUROSCI.23-24-08526.2003 Urbanchek, 1999, Rat walking tracks do not reflect maximal muscle force capacity, J. Reconstr. Microsurg., 15, 143, 10.1055/s-2007-1000085 Valero-Cabré, 2002, Functional impact of axonal misdirection after peripheral nerve injuries followed by graft or tube repair, J. Neurotrauma, 19, 1475, 10.1089/089771502320914705 Varejão, 2003, Toe out angle: a functional index for the evaluation of sciatic nerve recovery in the rat model, Exp. Neurol., 183, 695, 10.1016/S0014-4886(03)00208-5 Varejão, 2003, Ankle kinematics to evaluate functional recovery in crushed rat sciatic nerve, Muscle Nerve, 27, 706, 10.1002/mus.10374 Varejão, 2004, Methods for the experimental functional assessment of rat sciatic nerve regeneration, Neurol. Res., 26, 186, 10.1179/016164104225013833 Vleggeert-Lankamp, 2007, The role of evaluation methods in the assessment of peripheral nerve regeneration through synthetic conduits: a systematic review. Laboratory investigation, J. Neurosurg., 107, 1168, 10.3171/JNS-07/12/1168 Vogelaar, 2004, Sciatic nerve regeneration in mice and rats: recovery of sensory innervation is followed by a slowly retreating neuropathic pain-like syndrome, Brain Res., 1027, 67, 10.1016/j.brainres.2004.08.036 Walker, 1994, Gait-stance duration as a measure of injury and recovery in the rat sciatic nerve model, J. Neurosci. Methods, 52, 47, 10.1016/0165-0270(94)90054-X Wall, 1979, Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa, Pain, 7, 103, 10.1016/0304-3959(79)90002-2 Welt, 1990, Musculotopic organization of the facial motor nucleus in Macaca fascicularis: a morphometric and retrograde tracing study with cholera toxin B-HRP, J. Comp. Neurol., 291, 621, 10.1002/cne.902910409 Whitehead, 2005, Glial cell-line derived neurotrophic factor-dependent fusimotor neuron survival during development, Mech. Dev., 122, 27, 10.1016/j.mod.2004.09.003 Wolthers, 2005, Comparative electrophysiological, functional, and histological studies of nerve lesions in rats, Microsurgery, 25, 508, 10.1002/micr.20156 Xu, 2010, Motoneuron survival after chronic and sequential peripheral nerve injuries in the rat, J. Neurosurg., 112, 890, 10.3171/2009.8.JNS09812 Yeagle, 1983, Contractile properties of rat fast-twitch skeletal muscle during reinnervation: effects of testosterone and castration, Exp. Neurol., 82, 344, 10.1016/0014-4886(83)90407-7 Yu, 2001, Gait analysis in rats with peripheral nerve injury, Muscle Nerve, 24, 231, 10.1002/1097-4598(200102)24:2<231::AID-MUS80>3.0.CO;2-5