Therapeutic intraspinal stimulation to generate activity and promote long-term recovery

Frontiers in Neuroscience

Volumn , Issue 8 FEB, 2014, Pages

  Mondello, Sarah E ^a,b   Kasten, Michael R ^a   Horner, Philip J ^a,b   Moritz, Chet T ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Electrical activity; ISMS; Neuroprosthesis; Regenerative stimulation; Spinal cord injury

Indexed keywords

CELL SURVIVAL; CERVICAL INTRASPINAL MICROSTIMULATION; CERVICAL SPINAL CORD; CONVALESCENCE; DENDRITE; DEPTH ELECTRODE; ELECTRIC ACTIVITY; FORELIMB; HUMAN; LIMB MOVEMENT; MOTOR PERFORMANCE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE ELONGATION; NERVE FIBER GROWTH; NERVE SPROUTING; NERVOUS TISSUE; NEUROPROSTHESIS; NONHUMAN; NOTE; SPINAL CORD INJURY; SPINAL CORD STIMULATION; SYNAPTIC EFFICACY; SYNAPTOGENESIS;

EID: 84898044029     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00021     Document Type: Note

References (79)

1. Al-Majed, A. A., Brushart, T. M., and Gordon, T. (2000a). Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur. J. Neurosci. 12, 4381-4390. doi: 10.1111/j.1460-9568.2000.01341.x
2. Al-Majed, A. A., Neumann, C. M., Brushart, T. M., and Gordon, T. (2000b). Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J. Neurosci. 20, 2602-2608.
3. Al-Majed, A. A., Tam, S. L., and Gordon, T. (2004). Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell. Mol. Neurobiol. 24, 379-402. doi: 10.1023/B:CEMN.0000022770.66463.f7
4. Anderson, K. D. (2004). Targeting recovery: priorities of the spinal cord-injured population. J. Neurotrauma 21, 1371-1383. doi: 10.1089/neu.2004.21.1371
5. Balice-Gordon, R. J., and Lichtman, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524. doi: 10.1038/372519a0
6. Bamford, J. A., Todd, K. G., and Mushahwar, V. K. (2010). The effects of intraspinal microstimulation on spinal cord tissue in the rat. Biomaterials 31, 5552-5563. doi: 10.1016/j.biomaterials.2010.03.051
7. Barbeau, H., Ladouceur, M., Mirbagheri, M. M., and Kearney, R. E. (2002). The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies. Brain Res. Brain Res. Rev. 40, 274-291. doi: 10.1016/S0165-0173(02)00210-2
8. Bareyre, F. M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T. C., Weinmann, O., and Schwab, M. E. (2004). The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7, 269-277. doi: 10.1038/nn1195
9. Behrman, A. L., Nair, P. M., Bowden, M. G., Dauser, R. C., Herget, B. R., Martin, J. B., et al. (2008). Locomotor training restores walking in a nonambulatory child with chronic, severe, incomplete cervical spinal cord injury. Phys. Ther. 88, 580-590. doi: 10.2522/ptj.20070315
10. Borodinsky, L. N., Belgacem, Y. H., and Swapna, I. (2012). Electrical activity as a developmental regulator in the formation of spinal cord circuits. Curr. Opin. Neurobiol. 22, 624-630. doi: 10.1016/j.conb.2012.02.004
11. Brushart, T. M., Hoffman, P. N., Royall, R. M., Murinson, B. B., Witzel, C., and Gordon, T. (2002). Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J. Neurosci. 22, 6631-6638.
12. Brushart, T. M., Jari, R., Verge, V., Rohde, C., and Gordon, T. (2005). Electrical stimulation restores the specificity of sensory axon regeneration. Exp. Neurol. 194, 221-229. doi: 10.1016/j.expneurol.2005.02.007
13. Brus-Ramer, M., Carmel, J. B., Chakrabarty, S., and Martin, J. H. (2007). Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. J. Neurosci. 27, 13793-13801. doi: 10.1523/JNEUROSCI.3489-07.2007
14. Buffelli, M., Burgess, R. W., Feng, G., Lobe, C. G., Lichtman, J. W., and Sanes, J. R. (2003). Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424, 430-434. doi: 10.1038/nature01844
15. Carmel, J. B., Berrol, L. J., Brus-Ramer, M., and Martin, J. H. (2010). Chronic electrical stimulation of the intact corticospinal system after unilateral injury restores skilled locomotor control and promotes spinal axon outgrowth. J. Neurosci. 30, 10918-10926. doi: 10.1523/JNEUROSCI.1435-10.2010
16. Courtine, G., Song, B., Roy, R. R., Zhong, H., Herrmann, J. E., Ao, Y., et al. (2008). Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14, 69-74. doi: 10.1038/nm1682
17. Cox, S. B., Woolsey, T. A., and Rovainen, C. M. (1993). Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J. Cereb. Blood Flow Metab. 13, 899-913. doi: 10.1038/jcbfm.1993.113
18. Edgerton, V. R., and Harkema, S. (2011). Epidural stimulation of the spinal cord in spinal cord injury: current status and future challenges. Expert Rev. Neurother. 11, 1351-1353. doi: 10.1586/ern.11.129
19. Fenrich, K. K., and Rose, P. K. (2009). Spinal interneuron axons spontaneously regenerate after spinal cord injury in the adult feline. J. Neurosci. 29, 12145-12158. doi: 10.1523/JNEUROSCI.0897-09.2009
20. Foreman, R. D., and Linderoth, B. (2012). Neural mechanisms of spinal cord stimulation. Int. Rev. Neurobiol. 107, 87-119. doi: 10.1016/B978-0-12-404706-8.00006-1
21. Fox, E. J., Tester, N. J., Phadke, C. P., Nair, P. M., Senesac, C. R., Howland, D. R., et al. (2010). Ongoing walking recovery 2 years after locomotor training in a child with severe incomplete spinal cord injury. Phys. Ther. 90, 793-802. doi: 10.2522/ptj.20090171
22. Gerasimenko, Y., Roy, R. R., and Edgerton, V. R. (2008). Epidural stimulation: Comparison of the spinal circuits that generate and control locomotion in rats, cats and humans. Exp. Neurol. 209, 417-425. doi: 10.1016/j.expneurol.2007.07.015
23. Giszter, S. F., Mussa-Ivaldi, F. A., and Bizzi, E. (1993). Convergent force fields organized in the frog's spinal cord. J. Neurosci. 13, 467-491.
24. Goldberg, J. L., Espinosa, J. S., Xu, Y., Davidson, N., Kovacs, G. T., and Barres, B. A. (2002). Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33, 689-702. doi: 10.1016/S0896-6273(02)00602-5
25. Grumbles, R. M., Liu, Y., Thomas, C. M., Wood, P. M., and Thomas, C. K. (2013). Acute stimulation of transplanted neurons improves motoneuron survival, axon growth, and muscle reinnervation. J. Neurotrauma 30, 1062-1069. doi: 10.1089/neu.2012.2797
26. Hanson, M. G., and Landmesser, L. T. (2006). Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons. J. Neurosci. 26, 12769-12780. doi: 10.1523/JNEUROSCI.4170-06.2006
27. Harder, D. R., Roman, R. J., Gebremedhin, D., Birks, E. K., and Lange, A. R. (1998). A common pathway for regulation of nutritive blood flow to the brain: arterial muscle membrane potential and cytochrome P450 metabolites. Acta Physiol. Scand. 164, 527-532.
28. Harkema, S., Gerasimenko, Y., Hodes, J., Burdick, J., Angeli, C., Chen, Y., et al. (2011). Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 377, 1938-1947. doi: 10.1016/S0140-6736(11)60547-3
29. Hartshorn, D. O., Miller, J. M., and Altschuler, R. A. (1991). Protective effect of electrical stimulation in the deafened guinea pig cochlea. Otolaryngol. Head Neck Surg. 104, 311-319.
30. Herman, R., He, J., D'luzansky, S., Willis, W., and Dilli, S. (2002). Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured. Spinal Cord 40, 65-68. doi: 10.1038/sj.sc.3101263
31. Houle, J. D., Tom, V. J., Mayes, D., Wagoner, G., Phillips, N., and Silver, J. (2006). Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 26, 7405-7415. doi: 10.1523/JNEUROSCI.1166-06.2006
32. Iadecola, C., and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376. doi: 10.1038/nn2003
33. Ichiyama, R. M., Gerasimenko, Y. P., Zhong, H., Roy, R. R., and Edgerton, V. R. (2005). Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci. Lett. 383, 339-344. doi: 10.1016/j.neulet.2005.04.049
34. 2+ channel clustering in axon terminals disturbs excitability in motoneurons in spinal muscular atrophy. J. Cell Biol. 179, 139-149. doi: 10.1083/jcb.200703187
35. Jung, R., Belanger, A., Kanchiku, T., Fairchild, M., and Abbas, J. J. (2009). Neuromuscular stimulation therapy after incomplete spinal cord injury promotes recovery of interlimb coordination during locomotion. J. Neural Eng. 6:055010. doi: 10.1088/1741-2560/6/5/055010
36. Kasten, M. R., Sunshine, M. D., and Moritz, C. T. (2012). "Cervical intraspinal microstimulation improves forelimb motor recovery after spinal contusion injury," in International Functional Electrical Stimulation Society, (Banff, AB).
37. Kasten, M. R., Sunshine, M. D., Secrist, E. S., Horner, P. J., and Moritz, C. T. (2013). Therapeutic intraspinal microstimulation improves forelimb function after cervical contusion injury. J. Neural Eng. 10:044001. doi: 10.1088/1741-2560/10/4/044001
38. Leake, P. A., Hradek, G. T., Rebscher, S. J., and Snyder, R. L. (1991). Chronic intracochlear electrical stimulation induces selective survival of spiral ganglion neurons in neonatally deafened cats. Hear. Res. 54, 251-271. doi: 10.1016/0378-5955(91)90120-X
39. Lemay, M. A., and Grill, W. M. (2004). Modularity of motor output evoked by intraspinal microstimulation in cats. J. Neurophysiol. 91, 502-514. doi: 10.1152/jn.00235.2003
40. Leybaert, L. (2005). Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J. Cereb. Blood Flow Metab. 25, 2-16. doi: 10.1038/sj.jcbfm.9600001
41. Lohmann, C., Myhr, K. L., and Wong, R. O. (2002). Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418, 177-181. doi: 10.1038/nature00850
42. Lousteau, R. J. (1987). Increased spiral ganglion cell survival in electrically stimulated, deafened guinea pig cochleae. Laryngoscope 97, 836-842. doi: 10.1288/00005537-198707000-00012
43. Lu, J., Feron, F., Mackay-Sim, A., and Waite, P. M. (2002). Olfactory ensheathing cells promote locomotor recovery after delayed transplantation into transected spinal cord. Brain 125, 14-21. doi: 10.1093/brain/awf014
44. Malone, M., Gary, D., Yang, I. H., Miglioretti, A., Houdayer, T., Thakor, N., et al. (2013). Neuronal activity promotes myelination via a cAMP pathway. Glia 61, 843-854. doi: 10.1002/glia.22476
45. Mckenna, J. E., and Whishaw, I. Q. (1999). Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J. Neurosci. 19, 1885-1894.
46. Mctigue, D. M., Horner, P. J., Stokes, B. T., and Gage, F. H. (1998). Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18, 5354-5365.
47. Mirbagheri, M. M., Ladouceur, M., Barbeau, H., and Kearney, R. E. (2002). The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects. IEEE Trans. Neural Syst. Rehabil. Eng. 10, 280-289. doi: 10.1109/TNSRE.2002.806838
48. Morimoto, T., Jeffrey, L. G., and Ephraim, F. T. (2012). "Chapter Two-role of electrical activity of neurons for neuroprotection," in International Review of Neurobiology, eds J. L. Goldberg and E. F. Trakhtenberg (London; Amsterdam; Oxford; Waltham; San Diego: Academic Press), 19-38.
49. Moritz, C. T., Lucas, T. H., Perlmutter, S. I., and Fetz, E. E. (2007). Forelimb movements and muscle responses evoked by microstimulation of cervical spinal cord in sedated monkeys. J. Neurophysiol. 97, 110-120. doi: 10.1152/jn.00414.2006
50. Mushahwar, V. K., Aoyagi, Y., Stein, R. B., and Prochazka, A. (2004). Movements generated by intraspinal microstimulation in the intermediate gray matter of the anesthetized, decerebrate, and spinal cat. Can. J. Physiol. Pharmacol. 82, 702-714. doi: 10.1139/y04-079
51. Mushahwar, V. K., Collins, D. F., and Prochazka, A. (2000). Spinal cord microstimulation generates functional limb movements in chronically implanted cats. Exp. Neurol. 163, 422-429. doi: 10.1006/exnr.2000.7381
52. Mushahwar, V. K., Gillard, D. M., Gauthier, M. J., and Prochazka, A. (2002). Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements. IEEE Trans. Neural Syst. Rehabil. Eng. 10, 68-81. doi: 10.1109/TNSRE.2002.1021588
53. Mushahwar, V. K., and Horch, K. W. (1998). Selective activation and graded recruitment of functional muscle groups through spinal cord stimulation. Ann. N.Y. Acad. Sci. 860, 531-535. doi: 10.1111/j.1749-6632.1998.tb09096.x
54. Musienko, P., Van Den Brand, R., Marzendorfer, O., Roy, R. R., Gerasimenko, Y., Edgerton, V. R., et al. (2011). Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J. Neurosci. 31, 9264-9278. doi: 10.1523/JNEUROSCI.5796-10.2011
55. NSCISC. (2013). Spinal Cord Injury Facts and Figures at a Glance [Online]. Birmingham: The National Spinal Cord Injury Statistical Center. Available online at: https://www.nscisc.uab.edu/
56. Nutt, S. E., Chang, E. A., Suhr, S. T., Schlosser, L. O., Mondello, S. E., Moritz, C. T., et al. (2013). Caudalized human iPSC-derived neural progenitor cells produce neurons and glia but fail to restore function in an early chronic spinal cord injury model. Exp. Neurol. 248, 491-503. doi: 10.1016/j.expneurol.2013.07.010
57. Parr, A. M., Kulbatski, I., Zahir, T., Wang, X., Yue, C., Keating, A., et al. (2008). Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155, 760-770. doi: 10.1016/j.neuroscience.2008.05.042
58. Pearse, D. D., Pereira, F. C., Marcillo, A. E., Bates, M. L., Berrocal, Y. A., Filbin, M. T., et al. (2004). cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 10, 610-616. doi: 10.1038/nm1056
59. Petkau, T. L., Neal, S. J., Milnerwood, A., Mew, A., Hill, A. M., Orban, P., et al. (2012). Synaptic dysfunction in progranulin-deficient mice. Neurobiol. Dis. 45, 711-722. doi: 10.1016/j.nbd.2011.10.016
60. Petoukhov, E., Fernando, S., Mills, F., Shivji, F., Hunter, D., Krieger, C., et al. (2013). Activity-dependent secretion of progranulin from synapses. J. Cell Sci. 126, 5412-5421. doi: 10.1242/jcs.132076
61. Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., and Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251. doi: 10.1126/science.1072699
62. Qiu, J., Cai, D., Dai, H., Mcatee, M., Hoffman, P. N., Bregman, B. S., et al. (2002). Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34, 895-903. doi: 10.1016/S0896-6273(02)00730-4
63. Salimi, I., and Martin, J. H. (2004). Rescuing transient corticospinal terminations and promoting growth with corticospinal stimulation in kittens. J. Neurosci. 24, 4952-4961. doi: 10.1523/JNEUROSCI.0004-04.2004
64. Schrimsher, G. W., and Reier, P. J. (1992). Forelimb motor performance following cervical spinal cord contusion injury in the rat. Exp. Neurol. 117, 287-298. doi: 10.1016/0014-4886(92)90138-G
65. Shain, W., Spataro, L., Dilgen, J., Haverstick, K., Retterer, S., Isaacson, M., et al. (2003). Controlling cellular reactive responses around neural prosthetic devices using peripheral and local intervention strategies. IEEE Trans. Neural Syst. Rehabil. Eng. 11, 186-188. doi: 10.1109/TNSRE.2003.814800
66. Shen, S., Wiemelt, A. P., Mcmorris, F. A., and Barres, B. A. (1999). Retinal ganglion cells lose trophic responsiveness after axotomy. Neuron 23, 285-295. doi: 10.1016/S0896-6273(00)80780-1
67. Slawinska, U., Rossignol, S., Bennett, D. J., Schmidt, B. J., Frigon, A., Fouad, K., et al. (2012). Comment on "Restoring voluntary control of locomotion after paralyzing spinal cord injury." Science 338, 328. doi: 10.1126/science.1226082
68. Spataro, L., Dilgen, J., Retterer, S., Spence, A. J., Isaacson, M., Turner, J. N., et al. (2005). Dexamethasone treatment reduces astroglia responses to inserted neuroprosthetic devices in rat neocortex. Exp. Neurol. 194, 289-300. doi: 10.1016/j.expneurol.2004.08.037
69. Spitzer, N. C. (2006). Electrical activity in early neuronal development. Nature 444, 707-712. doi: 10.1038/nature05300
70. Sunshine, M. D., Cho, F. S., Lockwood, D. R., Fechko, A. S., Kasten, M. R., and Moritz, C. T. (2013). Cervical intraspinal microstimulation evokes robust forelimb movements before and after injury. J. Neural Eng. 10:036001. doi: 10.1088/1741-2560/10/3/036001
71. Tan, Y.-W., Zhang, S.-J., Hoffmann, T., and Bading, H. (2012). Increasing levels of wild-type CREB up-regulates several activity-regulated inhibitor of death (AID) genes and promotes neuronal survival. BMC Neurosci. 13:48. doi: 10.1186/1471-2202-13-48
72. Tapia, L., Milnerwood, A., Guo, A., Mills, F., Yoshida, E., Vasuta, C., et al. (2011). Progranulin deficiency decreases gross neural connectivity but enhances transmission at individual synapses. J. Neurosci. 31, 11126-11132. doi: 10.1523/JNEUROSCI.6244-10.2011
73. Tresch, M. C., and Bizzi, E. (1999). Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation. Exp. Brain Res. 129, 401-416. doi: 10.1007/s002210050908
74. Van Den Brand, R., Heutschi, J., Barraud, Q., Digiovanna, J., Bartholdi, K., Huerlimann, M., et al. (2012). Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 336, 1182-1185. doi: 10.1126/science.1217416
75. Wang, D., Ichiyama, R. M., Zhao, R., Andrews, M. R., and Fawcett, J. W. (2011). Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J. Neurosci. 31, 9332-9344. doi: 10.1523/JNEUROSCI.0983-11.2011
76. Yang, J. L., Lin, Y. T., Chuang, P. C., Bohr, V. A., and Mattson, M. P. (2013). BDNF and exercise enhance neuronal DNA repair by stimulating CREB-Mediated production of apurinic/apyrimidinic endonuclease 1. Neuromolecular Med. doi: 10.1007/s12017-013-8270-x. [Epub ahead of print].
77. Zhang, S. J., Steijaert, M. N., Lau, D., Schutz, G., Delucinge-Vivier, C., Descombes, P., et al. (2007). Decoding NMDA receptor signaling: identification of genomic programs specifying neuronal survival and death. Neuron 53, 549-562. doi: 10.1016/j.neuron.2007.01.025
78. Zheng, J. Q., Wan, J. J., and Poo, M. M. (1996). Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J. Neurosci. 16, 1140-1149.
79. Zimmermann, J. B., Seki, K., and Jackson, A. (2011). Reanimating the arm and hand with intraspinal microstimulation. J. Neural Eng. 8:054001. doi: 10.1088/1741-2560/8/5/054001