Enhancement of bilateral cortical somatosensory evoked potentials to intact forelimb stimulation following thoracic contusion spinal cord injury in rats

IEEE Transactions on Neural Systems and Rehabilitation Engineering

Volumn 22, Issue 5, 2014, Pages 953-964

  Bazley, Faith A ^a,b   Maybhate, Anil ^c   Tan, Chuen Seng ^b   Thakor, Nitish V ^a,b   Kerr, Candace ^d   All, Angelo H ^a,b,e  

^a Johns Hopkins University   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c Johns Hopkins University   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Contusion spinal cord injury; Cortical plasticity; Electrophysiology; Somatosensory evoked potentials; Unilateral spinal cord injury

Indexed keywords

CHEMICAL ACTIVATION; PATIENT REHABILITATION; RATS;

CENTRAL NERVOUS SYSTEMS; CORTICAL PLASTICITY; FUNCTIONAL RECOVERY; PRIMARY SOMATOSENSORY CORTEX; SOMATOSENSORY CORTEX; SOMATOSENSORY EVOKED POTENTIAL (SSEPS); SOMATOSENSORY EVOKED POTENTIALS; SPINAL CORD INJURIES (SCI);

ELECTROPHYSIOLOGY;

ANIMAL; CONTUSION; ELECTRODE IMPLANT; ELECTROSTIMULATION; EVOKED SOMATOSENSORY RESPONSE; FEMALE; FORELIMB; HEMISPHERIC DOMINANCE; INJURIES; LEWIS RAT; NERVE CELL PLASTICITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SPINAL CORD INJURY; VERTEBRA;

ANIMALS; CONTUSIONS; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; FORELIMB; FUNCTIONAL LATERALITY; MAGNETIC RESONANCE IMAGING; NEURONAL PLASTICITY; RATS; RATS, INBRED LEW; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 84920701178     PISSN: 15344320     EISSN: None     Source Type: Journal    
DOI: 10.1109/TNSRE.2014.2319313     Document Type: Article

References (47)

1. O. Raineteau and M. E. Schwab, "Plasticity of motor systems after incomplete spinal cord injury", Nature Rev. Neurosci., vol. 2, pp. 263-273, 2001.
2. K. Fouad, A. Krajacic, and W. Tetzlaff, "Spinal cord injury and plasticity: Opportunities and challenges", Brain Res. Bull., 2010.
3. S. M. Onifer, G. M. Smith, and K. Fouad, "Plasticity after spinal cord injury: Relevance to recovery and approaches to facilitate it", Neurotherapeutics, pp. 1-11, 2011.
4. G. Courtine, B. Song, R. R. Roy, H. Zhong, J. E. Herrmann, Y. Ao, J. Qi, V. R. Edgerton, and M. V. Sofroniew, "Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury", Nature Med., vol. 14, pp. 69-74, 2008.
5. A. Curt, H. J. A. Van Hedel, D. Klaus, and V. Dietz, "Recovery from a spinal cord injury: Significance of compensation, neural plasticity, and repair", J. Neurotrauma, vol. 25, pp. 677-685, 2008.
6. A. Blesch and M. H. Tuszynski, "Spinal cord injury: Plasticity, regeneration and the challenge of translational drug development", Trends Neurosci., vol. 32, pp. 41-47, 2009.
7. C. P. Hofstetter, P. Schweinhardt, T. Klason, L. Olson, and C. Spenger, "Numb rats walk-A behavioural and fMRI comparison of mild and moderate spinal cord injury", Eur. J. Neurosci., vol. 18, pp. 3061-3068, 2003.
8. J. Ramu, K. H. Bockhorst, R. J. Grill, K. V. Mogatadakala, and P. A. Narayana, "Cortical reorganization in NT3-treated experimental spinal cord injury: Functional magnetic resonance imaging", Exp. Neurol., vol. 204, pp. 58-65, 2007.
9. T. Endo, C. Spenger, T. Tominaga, S. Brené, and L. Olson, "Cortical sensory map rearrangement after spinal cord injury: fMRI responses linked to nogo signalling", Brain, vol. 130, pp. 2951-2961, 2007.
10. G. Agrawal, C. Kerr, N. V. Thakor, and A. H. All, "Characterization of graded multicenter animal spinal cord injury study contusion spinal cord injury using somatosensory-evoked potentials", Spine, vol. 35, pp. 1122-1127, May 2010.
11. M. Boakye, S. Harkema, P. H. Ellaway, and A. C. Skelly, "Quantitative testing in spinal cord injury: Overview of reliability and predictive validity", J. Neurosurg. Spine, vol. 17, pp. 141-150, 2012.
12. G. Agrawal, N. V. Thakor, and A. H. All, "Evoked potential versus behavior to detect minor insult to the spinal cord in a rat model", J. Clin. Neurosci., vol. 16, pp. 1052-1055, Aug. 2009.
13. A. H. All, F. A. Bazley, S. Gupta, N. Pashai, C. Hu, A. Pourmorteza, and C. Kerr, "Human embryonic stem cell-derived oligodendrocyte progenitors aid in functional recovery of sensory pathways following contusive spinal cord injury", PLoS ONE, vol. 7, p. e47645, 2012.
14. F. A. Bazley, C. Hu, A. Maybhate, A. Pourmorteza, N. Pashai, N. V. Thakor, C. L. Kerr, and A. H. All, "Electrophysiological evaluation of sensory and motor pathways after incomplete unilateral spinal cord contusion", J. Neurosurg. Spine, vol. 16, pp. 414-423, 2012.
15. A. H. All, P. Walczak, G. Agrawal, M. Gorelik, C. Lee, N. V. Thakor, J. W. M. Bulte, and D. A. Kerr, "Effect of MOG sensitization on somatosensory evoked potential in Lewis rats", J. Neurol. Sci., vol. 284, pp. 81-89, 2009.
16. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates. New York: Academic, 2006.
17. S. Iyer, A. Maybhate, A. Presacco, and A. H. All, "Multi-limb acquisition of motor evoked potentials and its application in spinal cord injury", J. Neurosci. Methods, vol. 193, pp. 210-216, 2010.
18. G. Agrawal, D. Sherman, A. Maybhate, M. Gorelik, D. A. Kerr, N. V. Thakor, and A. H. All, "Slope analysis of somatosensory evoked potentials in spinal cord injury for detecting contusion injury and focal demyelination", J. Clin. Neurosci., vol. 17, pp. 1159-1164, 2010.
19. G. Agrawal, D. Sherman, N. Thakor, and A. All, "A novel shape analysis technique for somatosensory evoked potentials", in Proc. IEEE Eng. Med. Biol. Soc. Conf., 2008, pp. 4688-4691.
20. A. H. All, G. Agrawal, P. Walczak, A. Maybhate, J. W. M. Bulte, and D. A. Kerr, "Evoked potential and behavioral outcomes for experimental autoimmune encephalomyelitis in Lewis rats", Neurol. Sci., vol. 31, pp. 595-601, 2010.
21. A. Maybhate, C. Hu, F. A. Bazley, Q. Yu, N. V. Thakor, C. L. Kerr, and A. H. All, "Potential long-term benefits of acute hypothermia after spinal cord injury: Assessments with somatosensory-evoked potentials", Crit. Care Med., vol. 40, p. 573, 2012.
22. F. A. Bazley, A. Pourmorteza, S. Gupta, N. Pashai, C. Kerr, and A. H. All, "DTI for assessing axonal integrity after contusive spinal cord injury and transplantation of oligodendrocyte progenitor cells", in Proc. IEEE Eng. Med. Biol. Soc. Conf., 2012, pp. 82-85.
23. J. Madhok, A. Maybhate, W. Xiong, M. A. Koenig, R. G. Geocadin, X. Jia, and N. V. Thakor, "Quantitative assessment of somatosensoryevoked potentials after cardiac arrest in rats: Prognostication of functional outcomes", Crit. Care Med., vol. 38, p. 1709, 2010.
24. T. Schallert, S. M. Fleming, J. L. Leasure, J. L. Tillerson, and S. T. Bland, "CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, Parkinsonism and spinal cord injury", Neuropharmacology, vol. 39, pp. 777-787, 2000.
25. F. A. Bazley, A. All, N. V. Thakor, and A. Maybhate, "Plasticity associated changes in cortical somatosensory evoked potentials following spinal cord injury in rats", in Proc. IEEE Eng. Med. Biol. Soc. Conf., Aug. 2011, pp. 2005-2008.
26. W. B. J. Cafferty, A. W. McGee, and S. M. Strittmatter, "Axonal growth therapeutics: Regeneration or sprouting or plasticity?", Trends Neurosci., vol. 31, pp. 215-220, 2008.
27. S. J. Harkema, "Plasticity of interneuronal networks of the functionally isolated human spinal cord", Brain Res. Rev., vol. 57, pp. 255-264, 2008.
28. V. R. Edgerton, N. J. K. Tillakaratne, A. J. Bigbee, R. D. De Leon, and R. R. Roy, "Plasticity of the spinal neural circuitry after injury", Annu. Rev. Neurosci., vol. 27, pp. 145-167, 2004.
29. V. Dietz, "Neuronal plasticity after a human spinal cord injury: Positive and negative effects", Exp. Neurol., vol. 235, no. 1, pp. 110-115, 2011.
30. R. Chaerkady, B. Letzen, S. Renuse, N. A. Sahasrabuddhe, P. Kumar, A. H. All, N. V. Thakor, B. Delanghe, J. D. Gearhart, and A. Pandey, "Quantitative temporal proteomic analysis of human embryonic stem cell differentiation into oligodendrocyte progenitor cells", Proteomics, vol. 11, no. 20, pp. 4007-4020, 2011.
31. C. L. Kerr, B. S. Letzen, C. M. Hill, G. Agrawal, N. V. Thakor, J. L. Sterneckert, J. D. Gearhart, and A. H. All, "Efficient differentiation of human embryonic stem cells into oligodendrocyte progenitors for application in a rat contusion model of spinal cord injury", Int. J. Neurosci., vol. 120, pp. 305-313, 2010.
32. B. S. Letzen, C. Liu, N. V. Thakor, J. D. Gearhart, A. H. All, and C. L. Kerr, "MicroRNA expression profiling of oligodendrocyte differentiation from human embryonic stem cells", PloS One, vol. 5, p. e10480, 2010.
33. E. Huebner and S. Strittmatter, "Axon regeneration in the peripheral and central nervous systems", Cell Biol. Axon, pp. 305-360, 2009.
34. M. J. De Vivo, "Epidemiology of traumatic spinal cord injury: Trends and future implications", Spinal Cord, vol. 50, no. 5, pp. 365-372, 2012.
35. A. Ghosh, F. Haiss, E. Sydekum, R. Schneider, M. Gullo, M. T. Wyss, T. Mueggler, C. Baltes, M. Rudin, and B. Weber, "Rewiring of hindlimb corticospinal neurons after spinal cord injury", Nature Neurosci., vol. 13, pp. 97-104, 2009.
36. E. Sydekum, C. Baltes, A. Ghosh, T. Mueggler, M. E. Schwab, and M. Rudin, "Functional reorganization in rat somatosensory cortex assessed by fMRI: Elastic image registration based on structural landmarks in fMRI images and application to spinal cord injured rats", Neuroimage, vol. 44, pp. 1345-1354, 2009.
37. J. Ramu, K. H. Bockhorst, K. V. Mogatadakala, and P. A. Narayana, "Functional magnetic resonance imaging in rodents: Methodology and application to spinal cord injury", J. Neurosci. Res., vol. 84, pp. 1235-1244, 2006.
38. J.-S. Rao, M. Manxiu, C. Zhao, Y. Xi, Z.-Y. Yang, L. Zuxiang, and X.-G. Li, "Atrophy and primary somatosensory cortical reorganization after unilateral thoracic spinal cord injury: A longitudinal functional magnetic resonance imaging study", BioMed Res. Int., vol. 2013.
39. M. P. Côté, M. R. Detloff, R. E. Wade, Jr., M. A. Lemay, and J. D. Houlé, "Plasticity in ascending long propriospinal and descending supraspinal pathways in chronic cervical spinal cord injured rats", Front. Physiol., vol. 3, 2012.
40. J. Yague, G. Foffani, and J. Aguilar, "Cortical hyperexcitability in response to preserved spinothalamic inputs immediately after spinal cord hemisection", Exp. Neurol., vol. 227, pp. 252-263, 2011.
41. F. A. Bazley, N. Pashai, C. Kerr, N. Thakor, and A. H. All, "A simple and effective semi-invasive method for inducing local hypothermia in rat spinal cord", in Proc. IEEE Eng. Med. Biol. Soc. Conf., 2013, pp. 6321-6324.
42. S. I. Hodgetts, P. J. Simmons, and G. W. Plant, "Human mesenchymal precursor cells (Stro-1?) from spinal cord injury patients improve functional recovery and tissue sparing in an acute spinal cord injury rat model", Cell Transplant., vol. 22, no. 3, pp. 383-412, 2012.
43. H. C. Chen, T. H. Fong, P. W. Hsu, and W. T. Chiu, "Multifaceted effects of rapamycin on functional recovery after spinal cord injury in rats through autophagy promotion, anti-inflammation, and neuroprotection", J. Surg. Res., vol. 197, no. 1, pp. e203-e210, 2012.
44. I. C. Maier, K. Baumann, M. Thallmair, O. Weinmann, J. Scholl, and M. E. Schwab, "Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury", J. Neurosci., vol. 28, pp. 9386-9403, 2008.
45. A. C. Fuzaro, C. T. Guerreiro, F. C. Galetti, R. B. V. M. Jucá, and J. E. Araujo, "Modified constraint-induced movement therapy and modified forced-use therapy for stroke patients are both effective to promote balance and gait improvements", Revista Brasileira de Fisioterapia, vol. 16, pp. 157-165, 2012.
46. R. Van Den Brand, J. Heutschi, Q. Barraud, J. Di Giovanna, K. Bartholdi, M. Huerlimann, L. Friedli, I. Vollenweider, E. M. Moraud, and S. Duis, "Restoring voluntary control of locomotion after paralyzing spinal cord injury", Science, vol. 336, pp. 1182-1185, 2012.
47. C. R. Battistuzzo, R. J. Callister, R. Callister, and M. P. Galea, "A systematic review of exercise training to promote locomotor recovery in animal models of spinal cord injury", J. Neurotrauma, vol. 29, pp. 1600-1613, 2012.