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Tail nerve electrical stimulation-induced walking training promotes restoration of locomotion and electrophysiology in rats with chronic spinal cord injury

DOI: 10.4236/wjns.2018.82012, PP. 124-145

Keywords: tail nerve electrical stimulation (TANES),electrophysiology,rat,spinal cord injury,autophagia,horizontal ladder rung walking test

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Abstract:

Functional recovery is the final goal in the treatment of spinal cord injury. However, to date, few treatment strategies have demonstrated significant locomotor improvement in animal experiments. By using tail nerve electrical stimulation (TANES) as an open-field locomotor training method combined with glial scar ablation and cell transplantation, we have successfully promoted locomotor recovery in rats with chronic spinal cord contusion injury. The purpose of the present study is to further investigate the mechanism of TANES and its effect on electrophysiology. Spinal cord segment T10 of female, adult Long-Evans rats was contused using the NYU impactor device with 25 mm height setting. After injury, rats were randomly divided into three groups. Group I was used as a control without any treatment, group II and group III were subjected to basic treatment including glial scar ablation and transplantation of olfactory lamina propria 6 weeks after injury, and group III received TANES-induced open-field locomotor training weekly after basic treatment. All animals were allowed to survive 22 weeks, except some rats which were transected. Basso, Beattie, and Bresnahan (BBB) open-field locomotor rating scale, horizontal ladder rung walking test, and electrophysiological tests were used to assess the restoration of functional behavior and conduction. Results showed that TANES significantly improves locomotor recovery and spinal cord conduction, reflex, as well as significantly reduces the occurrence of autophagia. Additionally, after transection, trained rats still maintained higher BBB score than that of control rats. This may be related to the activity-dependent plasticity promoted by TANES-induced locomotor training.

References

[1]  Barakat, D.J., Gaglani, S.M., Neravetla, S.R., Sanchez, A.R., Andrade, C.M., Pressman, Y., et al. (2005) Survival, Integration, and Axon Growth Support of Glia Transplanted into the Chronically Contused Spinal Cord. Cell Transplant, 14, 225-240.
https://doi.org/10.3727/000000005783983106
[2]  Tetzlaff, W., Okon, E.B., Karimi-Abdolrezaee, S., Hill, C.E., Sparling, J.S., Plemel, J.R., et al. (2011) A Systematic Review of Cellular Transplantation Therapies for Spinal Cord Injury. Journal of Neurotrauma, 28, 1611-1682.
https://doi.org/10.1089/neu.2009.1177
[3]  Zhang, S., Kluge, B., Huang, F., Nordstrom, T., Doolen, S., Gross, M., et al. (2007) Photochemical Scar Ablation in Chronically Contused Spinal Cord of Rat. Journal of Neurotrauma, 24, 411-420.
https://doi.org/10.1089/neu.2006.0065
[4]  Zhang, S.X., Huang, F.F., Gates, M., White, J. and Holmberg, E. (2011) Histological Repair of Damaged Spinal Cord Tissue from Chronic Contusion Injury of Rat: A LM Observation. Histology and Histopathology, 26, 45-58.
[5]  Zhang, S.X., Huang, F., Gates, M. and Holmberg, E.G. (2011) Scar Ablation Combined with LP/OEC Transplantation Promotes Anatomical Recovery and P0-Positive Myelination in Chronically Contused Spinal Cord of Rats. Brain Research, 1399, 1-14.
https://doi.org/10.1016/j.brainres.2011.05.005
[6]  Zhang, S.X., Huang, F.F., Gates, M., White, J. and Holmberg, E.G. (2010) Tail nerve Electrical Stimulation Induces Body Weight-Supported Stepping in Rats with Spinal Cord Injury. Journal of Neuroscience Methods, 187, 183-189.
https://doi.org/10.1016/j.jneumeth.2010.01.008
[7]  Zhang, S.X., Huang, F., Gates, M. and Holmberg, E.G. (2012) Tail Nerve Electrical Stimulation Combined with Scar Ablation and Neural Transplantation Promotes Locomotor Recovery in Rats with Chronically Contused Spinal Cord. Brain Research, 1456, 22-35.
https://doi.org/10.1016/j.brainres.2012.03.054
[8]  Zhang, S.X., Huang, F., Gates, M., Shen, X. and Holmberg, E.G. (2016) Early Application of Tail Nerve Electrical Stimulation-Induced Walking Training Promotes Locomotor Recovery in Rats with Spinal Cord Injury. Spinal Cord, 54, 942-946.
https://doi.org/10.1038/sc.2016.30
[9]  Molinari, M. (2009) Plasticity Properties of CPG Circuits in Humans: Impact on Gait Recovery. Brain Research Bulletin, 78, 22-25.
https://doi.org/10.1016/j.brainresbull.2008.02.030
[10]  Guertin, P.A. (2012) Central Pattern Generator for Locomotion: Anatomical, Physiological, and Pathophysiological Considerations. Frontiers in Neurology, 3, 183.
[11]  Wolpaw, J.R. (2007) Spinal Cord Plasticity in Acquisition and Maintenance of Motor Skills. Acta Physiologica, 189, 155-169.
https://doi.org/10.1111/j.1748-1716.2006.01656.x
[12]  Dunlop, S.A. (2008) Activity-Dependent Plasticity: Implications for Recovery after Spinal Cord Injury. Trends in Neurosciences, 31, 410-418.
https://doi.org/10.1016/j.tins.2008.05.004
[13]  Zhang, Y.T., Jin, H., Wang, J.H., Wen, L.Y., Yang, Y., Ruan, J.W., et al. (2017) Tail Nerve Electrical Stimulation and Electro-Acupuncture Can Protect Spinal Motor Neurons and Alleviate Muscle Atrophy after Spinal Cord Transection in Rats. Neural Plasticity, 2017, Article ID: 7351238.
[14]  Bazley, F.A., Hu, C., Maybhate, A., Pourmorteza, A., Pashai, N., Thakor, N.V., et al. (2012) Electrophysiological Evaluation of Sensory and Motor Pathways after Incomplete Unilateral Spinal Cord Contusion. Journal of Neurosurgery: Spine, 16, 414-423.
https://doi.org/10.3171/2012.1.SPINE11684
[15]  Constantini, S. and Young, W. (1994) The Effects of Methylprednisolone and the Ganglioside GM1 on Acute Spinal Cord Injury in Rats. Journal of Neurosurgery, 80, 97-111.
https://doi.org/10.3171/jns.1994.80.1.0097
[16]  Li, Y., Yu, H.L., Chen, L.F., Duan, C.X., Zhang, J.Y. and Li, B.C. (2010) Survival and Number of Olfactory Ensheathing Cells Transplanted in Contused Spinal Cord of Rats. Chinese Journal of Traumatology, 13, 356-361.
[17]  Basso, D.M., Beattie, M.S. and Bresnahan, J.C. (1995) A Sensitive and Reliable Locomotor Rating Scale for Open Field Testing in Rats. Journal of Neurotrauma, 12, 1-21.
https://doi.org/10.1089/neu.1995.12.1
[18]  Basso, D.M., Beattie, M.S. and Bresnahan, J.C. (1996) Graded Histological and Locomotor Outcomes after Spinal Cord Contusion Using the NYU Weight-Drop Device versus Transection. Experimental Neurology, 139, 244-256.
https://doi.org/10.1006/exnr.1996.0098
[19]  Metz, G.A. and Whishaw, I.Q. (2009) The Ladder Rung Walking Task: A Scoring System and Its Practical Application. Journal of Visualized Experiments, 28, e1204.
https://doi.org/10.3791/1204
[20]  Kunkel-Bagden, E., Dai, H.N. and Bregman, B.S. (1993) Methods to Assess the Development and Recovery of Locomotor Function after Spinal Cord Injury in Rats. Experimental Neurology, 119, 153-164.
https://doi.org/10.1006/exnr.1993.1017
[21]  Loy, D.N., Magnuson, D.S., Zhang, Y.P., Onifer, S.M., Mills, M.D., Cao, Q.L., et al. (2002) Functional Redundancy of Ventral Spinal Locomotor Pathways. Journal of Neuroscience, 22, 315-323.
https://doi.org/10.1523/JNEUROSCI.22-01-00315.2002
[22]  Metz, G.A. and Whishaw, I.Q. (2002) 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. Journal of Neuroscience Methods, 115, 169-179.
https://doi.org/10.1016/S0165-0270(02)00012-2
[23]  Zhang, S.X., Huang, F., Gates, M. and Holmberg, E.G. (2012) Somatosensory Evoked Potentials Can Be Recorded on the Midline of the Skull with Subdermal Electrodes in Non-Sedated Rats Elicited by Magnetic Stimulation of the Tibial Nerve. Journal of Neuroscience Methods, 208, 114-118.
https://doi.org/10.1016/j.jneumeth.2012.05.004
[24]  Linden, R.D., Zhang, Y.P., Burke, D.A., Hunt, M.A., Harpring, J.E. and Shields, C.B. (1999) Magnetic Motor Evoked Potential Monitoring in the Rat. Journal of Neurosurgery: Spine, 91, 205-210.
https://doi.org/10.3171/spi.1999.91.2.0205
[25]  Toleikis, J.R. (2005) Intraoperative Monitoring Using Somatosensory Evoked Potentials. A Position Statement by the American Society of Neurophysiological Monitoring. Journal of Clinical Monitoring and Computing, 19, 241-258.
https://doi.org/10.1007/s10877-005-4397-0
[26]  Zhang, Y.P., Shields, L.B., Zhang, Y., Pei, J., Xu, X.M., Hoskins, R., et al. (2007) Use of Magnetic Stimulation to Elicit Motor Evoked Potentials, Somatosensory Evoked Potentials, and H-Reflexes in Non-Sedated Rodents. Journal of Neuroscience Methods, 165, 9-17.
https://doi.org/10.1016/j.jneumeth.2007.05.021
[27]  Ferguson, A.R., Huie, J.R., Crown, E.D., Baumbauer, K.M., Hook, M.A., Garraway, S.M., et al. (2012) Maladaptive Spinal Plasticity Opposes Spinal Learning and Recovery in Spinal Cord Injury. Frontiers in Physiology, 3, 399.
https://doi.org/10.3389/fphys.2012.00399
[28]  Ferguson, A.R., Huie, J.R., Crown, E.D. and Grau, J.W. (2012) Central Nociceptive Sensitization vs. Spinal Cord Training: Opposing Forms of Plasticity that Dictate Function after Complete Spinal Cord Injury. Frontiers in Physiology, 3, 396.
https://doi.org/10.3389/fphys.2012.00396
[29]  Baumbauer, K.M., Turtle, J.D. and Grau, J.W. (2017) Fixed Spaced Stimulation Restores Adaptive Plasticity within the Spinal Cord: Identifying the Eliciting Conditions. Physiology & Behavior, 174, 1-9.
https://doi.org/10.1016/j.physbeh.2017.02.028
[30]  Zhang, S.X., Huang, F.F., Gates, M. and Holmberg, E. (2012) Tail Nerve Electrical Stimulation Combined with Scar Ablation and Neural Transplantation Improves Functional Recovery in Rats with Chronically Contused Spinal Cord. Journal of Neurotrauma, 29, No. 10.
[31]  McEwen, M.L. and Springer, J.E. (2006) Quantification of Locomotor Recovery Following Spinal Cord Contusion in Adult Rats. Journal of Neurotrauma, 23, 1632-1653.
https://doi.org/10.1089/neu.2006.23.1632
[32]  Wolpaw, J.R. and Tennissen, A.M. (2001) Activity-Dependent Spinal Cord Plasticity in Health and Disease. Annual Review of Neuroscience, 24, 807-843.
https://doi.org/10.1146/annurev.neuro.24.1.807
[33]  Garcia-Alias, G., Verdu, E., Fores, J., Lopez-Vales, R. and Navarro, X. (2003) Functional and Electrophysiological Characterization of Photochemical Graded Spinal Cord Injury in the Rat. Journal of Neurotrauma, 20, 501-510.
https://doi.org/10.1089/089771503765355568
[34]  Agrawal, G., Kerr, C., Thakor, N.V. and All, A.H. (2010) Characterization of Graded Multicenter Animal Spinal Cord Injury Study Contusion Spinal Cord Injury Using Somatosensory-Evoked Potentials. Spine, 35, 1122-1127.
https://doi.org/10.1097/BRS.0b013e3181be5fa7
[35]  Hu, Y., Wen, C.Y., Li, T.H., Cheung, M.M., Wu, E.X. and Luk K.D. (2011) Somatosensory-Evoked Potentials as an Indicator for the Extent of Ultrastructural Damage of the Spinal Cord after Chronic Compressive Injuries in a Rat Model. Clinical Neurophysiology, 122, 1440-1447.
https://doi.org/10.1016/j.clinph.2010.12.051
[36]  Valero-Cabre, A., Fores, J. and Navarro, X. (2004) Reorganization of Reflex Responses Mediated by Different Afferent Sensory Fibers after Spinal Cord Transection. Journal of Neurophysiology, 91, 2838-2848.
https://doi.org/10.1152/jn.01177.2003
[37]  Reese, N.B., Skinner, R.D., Mitchell, D., Yates, C., Barnes, C.N., Kiser, T.S., et al. (2006) Restoration of Frequency-Dependent Depression of the H-Reflex by Passive Exercise in Spinal Rats. Spinal Cord, 44, 28-34.
https://doi.org/10.1038/sj.sc.3101810
[38]  Skinner, R.D., Houle, J.D., Reese, N.B., Berry, C.L. and Garcia-Rill, E. (1996) Effects of Exercise and Fetal Spinal Cord Implants on the H-Reflex in Chronically Spinalized Adult Rats. Brain Research, 729, 127-131.
https://doi.org/10.1016/0006-8993(96)00556-2
[39]  Kiser, T.S., Reese, N.B., Maresh, T., Hearn, S., Yates, C., Skinner, R.D., et al. (2005) Use of a Motorized Bicycle Exercise Trainer to Normalize Frequency-Dependent Habituation of the H-Reflex in Spinal Cord Injury. Journal of Spinal Cord Medicine, 28, 241-245.
https://doi.org/10.1080/10790268.2005.11753818
[40]  Phadke, C.P., Flynn, S.M., Thompson, F.J., Behrman, A.L., Trimble, M.H. and Kukulka, C.G. (2009) Comparison of Single Bout Effects of Bicycle Training versus Locomotor Training on Paired Reflex Depression of the Soleus H-Reflex after Motor Incomplete Spinal Cord Injury. Archives of Physical Medicine and Rehabilitation, 90, 1218-1228.
https://doi.org/10.1016/j.apmr.2009.01.022
[41]  Cote, M.P., Amin, A.A., Tom, V.J. and Houle, J.D. (2011) Peripheral Nerve Grafts Support Regeneration after Spinal Cord Injury. Neurotherapeutics, 8, 294-303.
https://doi.org/10.1007/s13311-011-0024-6
[42]  Das, G.D., Das, K.G., Brasko, J., Riedl, M., Rai, P. and Rajeswari, V. (1989) Spinal Traumas: Some Postoperative Complications in Experimental Animals. Brain Research Bulletin, 22, 33-37.
https://doi.org/10.1016/0361-9230(89)90124-X
[43]  Mailis, A. (1996) Compulsive Targeted Self-Injurious Behaviour in Humans with Neuropathic Pain: A Counterpart of Animal Autotomy? Four Case Reports and Literature Review. PAIN, 64, 569-578.
https://doi.org/10.1016/0304-3959(95)00173-5
[44]  Frost, F.S., Mukkamala, S. and Covington, E. (2008) Self-Inflicted Finger Injury in Individuals with Spinal Cord Injury: An Analysis of 5 Cases. Journal of Spinal Cord Medicine, 31, 109-116.
https://doi.org/10.1080/10790268.2008.11753991

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