Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2017, Article ID 1932875, 15 pages
https://doi.org/10.1155/2017/1932875
Research Article

Following Spinal Cord Injury Transected Reticulospinal Tract Axons Develop New Collateral Inputs to Spinal Interneurons in Parallel with Locomotor Recovery

1Neuroscience and Mental Health Institute, University of Alberta, Edmonton, AB, Canada T6G 2E1
2Department of Physical Therapy, Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB, Canada T6G 2G4

Correspondence should be addressed to Karim Fouad; ac.atreblau@dauof.mirak

Received 8 March 2017; Revised 6 July 2017; Accepted 30 July 2017; Published 12 September 2017

Academic Editor: Michele Fornaro

Copyright © 2017 Zacnicte May et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. K. Park, K. Liu, Y. Hu et al., “Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway,” Science, vol. 322, no. 5903, pp. 963–966, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Caroni and M. E. Schwab, “Antibody against myelin associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter,” Neuron, vol. 1, no. 1, pp. 85–96, 1988. View at Publisher · View at Google Scholar · View at Scopus
  3. L. L. Jones, R. U. Margolis, and M. H. Tuszynski, “The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury,” Experimental Neurology, vol. 182, no. 2, pp. 399–411, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. Massey, C. H. Hubscher, M. R. Wagoner et al., “Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury,” Journal of Neuroscience, vol. 26, no. 16, pp. 4406–4414, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Ballermann and K. Fouad, “Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers,” The European Journal of Neuroscience, vol. 23, no. 8, pp. 1988–1996, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Fouad, V. Pedersen, M. E. Schwab, and C. Brösamle, “Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses,” Current Biology, vol. 11, no. 22, pp. 1766–1770, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Vavrek, J. Girgis, W. Tetzlaff, G. W. Hiebert, and K. Fouad, “BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats,” Brain, vol. 129, no. 6, pp. 1534–1545, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. F. M. Bareyre, M. Kerschensteiner, O. Raineteau, T. C. Mettenleiter, O. Weinmann, and M. E. Schwab, “The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats,” Nature Neuroscience, vol. 7, no. 3, pp. 269–277, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Filli, A. K. Engmann, B. Zorner et al., “Bridging the gap: a reticulo-propriospinal detour bypassing an incomplete spinal cord injury,” Journal of Neuroscience, vol. 34, no. 40, pp. 13399–13410, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. R. van den Brand, J. Heutschi, Q. Barraud et al., “Restoring voluntary control of locomotion after paralyzing spinal cord injury,” Science, vol. 336, no. 6085, pp. 1182–1185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Hayashi, T. Ueyama, K. Nemoto, T. Tamaki, and E. Senba, “Sequential mRNA expression for immediate early genes, cytokines, and neurotrophins in spinal cord injury,” Journal of Neurotrauma, vol. 17, no. 3, pp. 203–218, 2000. View at Publisher · View at Google Scholar
  12. K. C. Murray, A. Nakae, M. J. Stephens et al., “Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors,” Nature Medicine, vol. 16, no. 6, pp. 694–700, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. N. J. Tillakaratne, M. Mouria, N. B. Ziv, R. R. Roy, V. R. Edgerton, and A. J. Tobin, “Increased expression of glutamate decarboxylase (GAD(67)) in feline lumbar spinal cord after complete thoracic spinal cord transection,” Journal of Neuroscience Research, vol. 60, no. 2, pp. 219–230, 2000. View at Publisher · View at Google Scholar
  14. G. García-Alías, S. Barkhuysen, M. Buckle, and J. W. Fawcett, “Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation,” Nature Neuroscience, vol. 12, no. 9, pp. 1145–1151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. J. H. Martin, “The corticospinal system: from development to motor control,” The Neuroscientist, vol. 11, no. 2, pp. 161–173, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. R. N. Lemon, R. S. Johansson, and G. Westling, “Corticospinal control during reach, grasp, and precision lift in man,” Journal of Neuroscience, vol. 15, no. 9, pp. 6145–6156, 1995. View at Google Scholar
  17. C. E. Lang, “Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract,” Journal of Neurophysiology, vol. 91, no. 4, pp. 1722–1733, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. D. M. Basso, M. S. Beattie, and J. C. Bresnahan, “Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection,” Experimental Neurology, vol. 139, no. 2, pp. 244–256, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Schucht, O. Raineteau, M. E. Schwab, and K. Fouad, “Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord,” Experimental Neurology, vol. 176, no. 1, pp. 143–153, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. J. D. Steeves and L. M. Jordan, “Localization of a descending pathway in the spinal cord which is necessary for controlled treadmill locomotion,” Neuroscience Letters, vol. 20, no. 3, pp. 283–288, 1980. View at Google Scholar
  21. M. H. Tuszynski and O. Steward, “Concepts and methods for the study of axonal regeneration in the CNS,” Neuron, vol. 74, no. 5, pp. 777–791, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Vavrek, D. D. Pearse, and K. Fouad, “Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection,” Journal of Neurotrauma, vol. 24, no. 10, pp. 1667–1673, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. X. M. Xu, V. Guénard, N. Kleitman, P. Aebischer, and M. B. Bunge, “A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord,” Experimental Neurology, vol. 134, no. 2, pp. 261–272, 1995. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Filli and M. Schwab, “Structural and functional reorganization of propriospinal connections promotes functional recovery after spinal cord injury,” Neural Regeneration Research, vol. 10, no. 4, p. 509, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Li, A. M. Lucas-Osma, S. Black et al., “Pericytes impair capillary blood flow and motor function after chronic spinal cord injury,” Nature Medicine, vol. 23, no. 6, pp. 733–741, 2017. View at Publisher · View at Google Scholar
  26. D. M. Basso, M. S. Beattie, and J. C. Bresnahan, “A sensitive and reliable locomotor rating scale for open field testing in rats,” Journal of Neurotrauma, vol. 12, no. 1, pp. 1–21, 1995. View at Publisher · View at Google Scholar
  27. G. Paxinos and C. Watson, The rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA, USA, 1998.
  28. W. R. Reed, A. Shum-Siu, and D. S. K. Magnuson, “Reticulospinal pathways in the ventrolateral funiculus with terminations in the cervical and lumbar enlargements of the adult rat spinal cord,” Neuroscience, vol. 151, no. 2, pp. 505–517, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. K. K. Fenrich, N. Skelton, V. E. MacDermid et al., “Axonal regeneration and development of de novo axons from distal dendrites of adult feline commissural interneurons after a proximal axotomy,” The Journal of Comparative Neurology, vol. 502, no. 6, pp. 1079–1097, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Grande, S. Armstrong, M. Neuber-Hess, and P. K. Rose, “Distribution of contacts from vestibulospinal axons on the dendrites of splenius motoneurons,” The Journal of Comparative Neurology, vol. 491, no. 4, pp. 339–351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Grande, T. V. Bui, and P. K. Rose, “Distribution of vestibulospinal contacts on the dendrites of ipsilateral splenius motoneurons: an anatomical substrate for push-pull interactions during vestibulocollic reflexes,” Brain Research, vol. 1333, pp. 9–27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Maratta, K. K. Fenrich, E. Zhao, M. S. Neuber-Hess, and P. K. Rose, “Distribution and density of contacts from noradrenergic and serotonergic boutons on the dendrites of neck flexor motoneurons in the adult cat: NA and 5-HT contacts on flexor motoneurons,” Journal of Comparative Neurology, vol. 523, no. 11, pp. 1701–1716, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. S. J. Montague, K. K. Fenrich, C. Mayer-Macaulay, R. Maratta, M. S. Neuber-Hess, and P. K. Rose, “Nonuniform distribution of contacts from noradrenergic and serotonergic boutons on the dendrites of cat splenius motoneurons,” Journal of Comparative Neurology, vol. 521, no. 3, pp. 638–656, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. F. J. Alvarez, J. C. Pearson, D. Harrington, D. Dewey, L. Torbeck, and R. E. W. Fyffe, “Distribution of 5-hydroxytryptamine-immunoreactive boutons on?-motoneurons in the lumbar spinal cord of adult cats,” The Journal of Comparative Neurology, vol. 393, no. 1, pp. 69–83, 1998. View at Publisher · View at Google Scholar
  35. R. E. Fyffe, “Spatial distribution of recurrent inhibitory synapses on spinal motoneurons in the cat,” Journal of Neurophysiology, vol. 65, no. 5, pp. 1134–1149, 1991. View at Google Scholar
  36. J. Lübke, V. Egger, B. Sakmann, and D. Feldmeyer, “Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex,” Journal of Neuroscience, vol. 20, no. 14, pp. 5300–5311, 2000. View at Google Scholar
  37. H. Markram, J. Lübke, M. Frotscher, A. Roth, and B. Sakmann, “Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex,” The Journal of Physiology, vol. 500, no. 2, pp. 409–440, 1997. View at Publisher · View at Google Scholar
  38. P. K. Rose, S. Ely, V. Norkum, and M. Neuber-Hess, “Projections from the lateral vestibular nucleus to the upper cervical spinal cord of the cat: a correlative light and electron microscopic study of axon terminals stained with PHA-L,” The Journal of Comparative Neurology, vol. 410, no. 4, pp. 571–585, 1999. View at Google Scholar
  39. R. A. Silver, “High-probability Uniquantal transmission at excitatory synapses in barrel cortex,” Science, vol. 302, no. 5652, pp. 1981–1984, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. S. W. Cha and C. K. Tan, “Projection of forelimb nerve afferents to external cuneate nucleus of the rat as revealed by intraneural injection of a neurotoxic lectin, Ricinus Communis agglutinin,” Histology and Histopathology, vol. 11, no. 1, pp. 117–123, 1996. View at Google Scholar
  41. A. M. Graybiel and E. A. Hartwieg, “Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques,” Brain Research, vol. 81, no. 3, pp. 543–551, 1974. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Jasmin and J. Courville, “Distribution of external cuneate nucleus afferents to the cerebellum: I. Notes on the projections from the main cuneate and other adjacent nuclei An experimental study with radioactive tracers in the cat,” The Journal of Comparative Neurology, vol. 261, no. 4, pp. 481–496, 1987. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Rea, “Spinal tracts-descending/motor pathways,” in Essential Clinical Anatomy of the Nervous System, pp. 161–176, Elsevier, Cambridge, MA, USA, 2015. View at Publisher · View at Google Scholar
  44. J. B. Travers, J.-E. Yoo, R. Chandran, K. Herman, and S. P. Travers, “Neurotransmitter phenotypes of intermediate zone reticular formation projections to the motor trigeminal and hypoglossal nuclei in the rat,” The Journal of Comparative Neurology, vol. 488, no. 1, pp. 28–47, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. D. N. Loy, D. S. Magnuson, Y. P. Zhang et al., “Functional redundancy of ventral spinal locomotor pathways,” Journal of Neuroscience, vol. 22, no. 1, pp. 315–323, 2002. View at Google Scholar
  46. Z. H. Kiss and C. H. Tator, “Neurogenic shock,” Shock and Resuscitation, McGraw Hill, New York, NY, USA, 1993. View at Google Scholar
  47. B. Sist, K. Fouad, and I. R. Winship, “Plasticity beyond peri-infarct cortex: spinal up regulation of structural plasticity, neurotrophins, and inflammatory cytokines during recovery from cortical stroke,” Experimental Neurology, vol. 252, pp. 47–56, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. K. L. Caudle, E. H. Brown, A. Shum-Siu et al., “Hindlimb immobilization in a wheelchair alters functional recovery following contusive spinal cord injury in the adult rat,” Neurorehabilitation and Neural Repair, vol. 25, no. 8, pp. 729–739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Ying, R. R. Roy, V. R. Edgerton, and F. Gómez-Pinilla, “Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury,” Experimental Neurology, vol. 193, no. 2, pp. 411–419, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Martinez, H. Delivet-Mongrain, H. Leblond, and S. Rossignol, “Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry,” Journal of Neurophysiology, vol. 108, no. 1, pp. 124–134, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Singh, S. Balasubramanian, M. Murray, M. Lemay, and J. Houle, “Role of spared pathways in locomotor recovery after body-weight-supported treadmill training in contused rats,” Journal of Neurotrauma, vol. 28, no. 12, pp. 2405–2416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Rossignol, T. Drew, E. Brustein, and W. Jiang, “Locomotor performance and adaptation after partial or complete spinal cord lesions in the cat,” Progress in Brain Research, vol. 123, pp. 349–365, 1999. View at Google Scholar
  53. O. Alluin, H. Delivet-Mongrain, and S. Rossignol, “Inducing hindlimb motor recovery in adult rat after complete thoracic spinal cord section using repeated treadmill training with perineal stimulation only,” Journal of Neurophysiology, vol. 114, no. 3, pp. 1931–1946, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Courtine, B. Song, R. R. Roy et al., “Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury,” Nature Medicine, vol. 14, no. 1, pp. 69–74, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Kinoshita, R. Matsui, S. Kato et al., “Genetic dissection of the circuit for hand dexterity in primates,” Nature, vol. 487, no. 7406, pp. 235–238, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. B. J. Hilton, E. Anenberg, T. C. Harrison, J. D. Boyd, T. H. Murphy, and W. Tetzlaff, “Re-establishment of cortical motor output maps and spontaneous functional recovery via spared Dorsolaterally projecting corticospinal neurons after dorsal column spinal cord injury in adult mice,” Journal of Neuroscience, vol. 36, no. 14, pp. 4080–4092, 2016. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Cowley, E. Zaporozhets, and B. Schmidt, “Propriospinal neurons are sufficient for bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord,” Journal of Physiology, vol. 586, no. 6, pp. 1623–1635, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Drew and S. Rossignol, “Functional organization within the medullary reticular formation of intact unanesthetized cat II. Electromyographic activity evoked by microstimulation,” Journal of Neurophysiology, vol. 64, no. 3, pp. 782–795, 1990. View at Google Scholar
  59. K. K. Fenrich and P. K. Rose, “Spinal interneuron axons spontaneously regenerate after spinal cord injury in the adult feline,” Journal of Neuroscience, vol. 29, no. 39, pp. 12145–12158, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. Goulding, “Circuits controlling vertebrate locomotion: moving in a new direction,” Nature Reviews Neuroscience, vol. 10, pp. 507–518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. Siegel, “Behavioral functions of the reticular formation,” Brain Research Reviews, vol. 1, pp. 69–105, 1979. View at Publisher · View at Google Scholar · View at Scopus
  62. S. G. Kanagal and G. D. Muir, “Task-dependent compensation after pyramidal tract and dorsolateral spinal lesions in rats,” Experimental Neurology, vol. 216, no. 1, pp. 193–206, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. O. Raineteau and M. E. Schwab, “Plasticity of motor systems after incomplete spinal cord injury,” Nature Reviews Neuroscience, vol. 2, no. 4, pp. 263–273, 2001. View at Publisher · View at Google Scholar · View at Scopus