Relationship between structural brainstem and brain plasticity and lower-limb training in spinal cord injury: A longitudinal pilot study

Frontiers in Human Neuroscience

Volumn 9, Issue MAY, 2015, Pages

  Villiger, Michael ^a,b   Grabher, Patrick ^a   Hepp Reymond, Marie Claude ^a   Kiper, Daniel ^a   Curt, Armin ^a   Bolliger, Marc ^a   Hotz Boendermaker, Sabina ^a   Kollias, Spyros ^c   Eng, Kynan ^a   Freund, Patrick ^a,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b University College Physiotherapy Thim Van der Laan   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Lower limb; Spinal cord injury; Structural plasticity; Tensor based morphometry; Virtual reality augmented neurorehabilitation; Voxel based morphometry

Indexed keywords

ADULT; AGED; ARTICLE; BODY EQUILIBRIUM; BRAIN SIZE; BRAIN STEM; CEREBELLUM; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CORPUS CALLOSUM; CORTICAL THICKNESS (BRAIN); DISEASE ASSOCIATION; FEMALE; FOLLOW UP; FUNCTIONAL TRAINING; FUSIFORM GYRUS; HUMAN; INCOMPLETE SPINAL CORD INJURY; LONGITUDINAL STUDY; MALE; MIDDLE AGED; MIDDLE OCCIPITAL GYRUS; MIDDLE TEMPORAL GYRUS; MOBILIZATION; MORPHOMETRICS; MOTOR CONTROL; MUSCLE STRENGTH; NERVE CELL PLASTICITY; PILOT STUDY; PRIMARY MOTOR CORTEX; REHABILITATION CARE; SPINAL CORD INJURY; TENSOR BASED MORPHOMETRY; TREATMENT DURATION; VIRTUAL REALITY; VOXEL BASED MORPHOMETRY; WALKING SPEED; WHITE MATTER;

EID: 84933678662     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2015.00254     Document Type: Article

References (55)

1. Adamovich, S. V., Fluet, G. G., Tunik, E., and Merians, A. S. (2009). Sensorimotor training in virtual reality: a review. NeuroRehabilitation 25, 29-44. doi: 10.3233/NRE-2009-0497
2. Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., et al. (2008). Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 58, 261-272. doi: 10.1016/j.neuron.2008.02.008
3. Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage38, 95-113. doi: 10.1016/j.neuroimage.2007.07.007
4. Ashburner, J., and Friston, K. J. (2000). Voxel-based morphometry-the methods.Neuroimage 11, 805-821. doi: 10.1006/nimg.2000.0582
5. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neuroimage 26, 839-851. doi: 10.1016/j.neuroimage.2005.02.018
6. Ashburner, J., and Ridgway, G. R. (2013). Symmetric diffeomorphic modeling of longitudinal structural MRI. Front. Neurosci. 6:197. doi: 10.3389/fnins.2012.00197
7. Berg, K., Wood-Dauphinee, S., and Williams, J. I. (1995). The balance scale: reliability assessment with elderly residents and patients with an acute stroke. Scand. J. Rehabil. Med. 27, 27-36.
8. Bohil, C. J., Alicea, B., and Biocca, F. A. (2011). Virtual reality in neuroscience research and therapy. Nat. Rev. Neurosci. 12, 752-762. doi: 10.1038/nrn3122
9. Bryce, T. N., Biering-Sørensen, F., Finnerup, N. B., Cardenas, D. D., Defrin, R., Ivan, E., et al. (2012). International Spinal Cord Injury Pain (ISCIP) classification: part 2. Initial validation using vignettes. Spinal Cord 50, 404-412. doi: 10.1038/sc.2012.2
10. Burciu, R. G., Fritsche, N., Granert, O., Schmitz, L., Spönemann, N., Konczak, J., et al. (2013). Brain changes associated with postural training in patients with cerebellar degeneration: a voxel-based morphometry study. J. Neurosci. 33, 4594-4604. doi: 10.1523/JNEUROSCI.3381-12.2013
11. Catz, A., Itzkovich, M., Tesio, L., Biering-Sorensen, F., Weeks, C., Laramee, M. T., et al. (2007). A multicenter international study on the spinal cord independence measure, version III: Rasch psychometric validation. Spinal Cord 45, 275-291. doi: 10.1038/sj.sc.3101960
12. Classen, J., Liepert, J., Wise, S. P., Hallett, M., and Cohen, L. G. (1998). Rapid plasticity of human cortical movement representation induced by practice. J. Neurophysiol. 79, 1117-1123.
13. Cohen-Adad, J., El Mendili, M. M., Lehéricy, S., Pradat, P. F., Blancho, S., Rossignol, S., et al. (2011). Demyelination and degeneration in the injured human spinal cord detected with diffusion and magnetization transfer MRI. Neuroimage 55, 1024-1033. doi: 10.1016/j.neuroimage.2010.11.089
14. Deliagina, T. G., Beloozerova, I. N., Zelenin, P. V., and Orlovsky, G. N. (2008). Spinal and supraspinal postural networks. Brain Res. Rev. 57, 212-221. doi: 10.1016/j.brainresrev.2007.06.017
15. Draganski, B., Gaser, C., Busch, V., Schuierer, G., Bogdahn, U., and May, A. (2004). Neuroplasticity: changes in grey matter induced by training. Nature 427, 311-312. doi: 10.1038/427311a
16. Draganski, B., and May, A. (2008). Training-induced structural changes in the adult human brain. Behav. Brain Res. 192, 137-142. doi: 10.1016/j.bbr.2008.02.015
17. Driemeyer, J., Boyke, J., Gaser, C., Büchel, C., and May, A. (2008). Changes in gray matter induced by learning-revisited. PLoS One 3:e2669. doi: 10.1371/journal.pone.0002669
18. Freund, P., Schneider, T., Nagy, Z., Hutton, C., Weiskopf, N., Friston, K., et al. (2012a). Degeneration of the injured cervical cord is associated with remote changes in corticospinal tract integrity and upper limb impairment. PLoS One 7:e51729. doi: 10.1371/journal.pone.0051729
19. Freund, P., Weiskopf, N., Ashburner, J., Wolf, K., Sutter, R., Altmann, D. R., et al. (2013). MRI investigation of the sensorimotor cortex and the corticospinal tract after acute spinal cord injury: a prospective longitudinal study. Lancet Neurol. 12, 873-881. doi: 10.1016/s1474-4422(13)70146-7
20. Freund, P., Weiskopf, N., Ward, N. S., Hutton, C., Gall, A., Ciccarelli, O., et al. (2011). Disability, atrophy and cortical reorganization following spinal cord injury. Brain 134, 1610-1622. doi: 10.1093/brain/awr093
21. Freund, P., Wheeler-Kingshott, C. A., Nagy, Z., Gorgoraptis, N., Weiskopf, N., Friston, K., et al. (2012b). Axonal integrity predicts cortical reorganisation following cervical injury. J. Neurol. Neurosurg. Psychiatry 83, 629-637. doi: 10.1136/jnnp-2011-301875
22. Furlan, J. C., Bracken, M. B., and Fehlings, M. G. (2010). Is age a key determinant of mortality and neurological outcome after acute traumatic spinal cord injury?Neurobiol. Aging 31, 434-446. doi: 10.1016/j.neurobiolaging.2008.05.003
23. Ghosh, A., Haiss, F., Sydekum, E., Schneider, R., Gullo, M., Wyss, M. T., et al. (2010). Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat. Neurosci. 13, 97-104. doi: 10.1038/nn.2448
24. Hassanpour, K., Hotz-Boendermaker, S., Dokladal, P., European Multicenter Study for Human Spinal Cord Injury Study group, and Curt, A. (2012). Low depressive symptoms in acute spinal cord injury compared to other neurological disorders. J. Neurol. 259, 1142-1150. doi: 10.1007/s00415-011-6316-2
25. Holden, M. K. (2005). Virtual environments for motor rehabilitation: review.Cyberpsychol. Behav. 8, 187-211; discussion 212-219. doi: 10.1089/cpb.2005.8.187
26. Houk, J. C., Buckingham, J. T., and Barto, A. G. (1996). Models of the cerebellum and motor learning. Behav. Brain Sci. 19, 368-383. doi: 10.1017/S0140525X00081474
27. Hua, X., Hibar, D. P., Ching, C. R., Boyle, C. P., Rajagopalan, P., Gutman, B. A., et al. (2013). Unbiased tensor-based morphometry: improved robustness and sample size estimates for Alzheimer's disease clinical trials. Neuroimage 66, 648-661. doi: 10.1016/j.neuroimage.2012.10.086
28. Hutton, C., De Vita, E., Ashburner, J., Deichmann, R., and Turner, R. (2008). Voxel-based cortical thickness measurements in MRI. Neuroimage 40, 1701-1710. doi: 10.1016/j.neuroimage.2008.01.027
29. Hutton, C., Draganski, B., Ashburner, J., and Weiskopf, N. (2009). A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. Neuroimage 48, 371-380. doi: 10.1016/j.neuroimage.2009.06.043
30. Kantak, S. S., Jones-Lush, L. M., Narayanan, P., Judkins, T. N., and Wittenberg, G. F. (2013). Rapid plasticity of motor corticospinal system with robotic reach training.Neuroscience 247, 55-64. doi: 10.1016/j.neuroscience.2013.05.001
31. Koeneke, S., Lutz, K., Herwig, U., Ziemann, U., and Jäncke, L. (2006). Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp. Brain Res. 174, 199-209. doi: 10.1007/s00221-006-0440-8
32. Landi, S. M., Baguear, F., and Della-Maggiore, V. (2011). One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory one year later. J. Neurosci. 31, 11808-11813. doi: 10.1523/JNEUROSCI.2253-11.2011
33. Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S., et al. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. U S A 97, 4398-4403. doi: 10.1073/pnas.070039597
34. Marino, R. J., Barros, T., Biering-Sorensen, F., Burns, S. P., Donovan, W. H., Graves, D. E., et al. (2003). International standards for neurological classification of spinal cord injury. J. Spinal Cord Med. 26, 50-56.
35. Markham, J. A., and Greenough, W. T. (2004). Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 1, 351-363. doi: 10.1017/s1740925x05000219
36. Moseley, G. L. (2007). Using visual illusion to reduce at-level neuropathic pain in paraplegia. Pain 130, 294-298. doi: 10.1016/j.pain.2007.01.007
37. Pascual-Leone, A., Nguyet, D., Cohen, L. G., Brasil-Neto, J. P., Cammarota, A., and Hallett, M. (1995). Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J. Neurophysiol. 74, 1037-1045.
38. Perez, M. A., Lungholt, B. K., Nyborg, K., and Nielsen, J. B. (2004). Motor skill training induces changes in the excitability of the leg cortical area in healthy humans.Exp. Brain Res. 159, 197-205. doi: 10.1007/s00221-004-1947-5
39. Quallo, M. M., Price, C. J., Ueno, K., Asamizuya, T., Cheng, K., Lemon, R. N., et al. (2009). Gray and white matter changes associated with tool-use learning in macaque monkeys. Proc. Natl. Acad. Sci. U S A 106, 18379-18384. doi: 10.1073/pnas.0909751106
40. Rabe, K., Livne, O., Gizewski, E. R., Aurich, V., Beck, A., Timmann, D., et al. (2009). Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. J. Neurophysiol. 101, 1961-1971. doi: 10.1152/jn.91069.2008
41. Sagi, Y., Tavor, I., Hofstetter, S., Tzur-Moryosef, S., Blumenfeld-Katzir, T., and Assaf, Y. (2012). Learning in the fast lane: new insights into neuroplasticity. Neuron 73, 1195-1203. doi: 10.3410/f.717952851.793458334
42. Sampaio-Baptista, C., Filippini, N., Stagg, C. J., Near, J., Scholz, J., and Johansen-Berg, H. (2015). Changes in functional connectivity and GABA levels with long-term motor learning. Neuroimage 106, 15-20. doi: 10.1016/j.neuroimage.2014.11.032
43. Schendan, H. E., Searl, M. M., Melrose, R. J., and Stern, C. E. (2003). An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning.Neuron 37, 1013-1025. doi: 10.1016/s0896-6273(03)00123-5
44. Sehm, B., Taubert, M., Conde, V., Weise, D., Classen, J., Dukart, J., et al. (2014). Structural brain plasticity in Parkinson's disease induced by balance training.Neurobiol. Aging 35, 232-239. doi: 10.1016/j.neurobiolaging.2013.06.021
45. Tao, G., Datta, S., He, R., Nelson, F., Wolinsky, J. S., and Narayana, P. A. (2009). Deep gray matter atrophy in multiple sclerosis: a tensor based morphometry. J. Neurol. Sci. 282, 39-46. doi: 10.1016/j.jns.2008.12.035
46. Taubert, M., Draganski, B., Anwander, A., Müller, K., Horstmann, A., Villringer, A., et al. (2010). Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J. Neurosci. 30, 11670-11677. doi: 10.1523/JNEUROSCI.2567-10.2010
47. Taubert, M., Lohmann, G., Margulies, D. S., Villringer, A., and Ragert, P. (2011). Long-term effects of motor training on resting-state networks and underlying brain structure. Neuroimage 57, 1492-1498. doi: 10.1016/j.neuroimage.2011.05.078
48. Tessa, C., Lucetti, C., Giannelli, M., Diciotti, S., Poletti, M., Danti, S., et al. (2014). Progression of brain atrophy in the early stages of Parkinson's disease: a longitudinal tensor-based morphometry study in de novo patients without cognitive impairment.Hum. Brain Mapp. 35, 3932-3944. doi: 10.1002/hbm.22449
49. van Hedel, H. J., Wirz, M., and Curt, A. (2006). Improving walking assessment in subjects with an incomplete spinal cord injury: responsiveness. Spinal Cord 44, 352-356. doi: 10.1038/sj.sc.3101853
50. van Hedel, H. J., Wirz, M., and Dietz, V. (2005). Assessing walking ability in subjects with spinal cord injury: validity and reliability of 3 walking tests. Arch. Phys. Med. Rehabil. 86, 190-196. doi: 10.1016/j.apmr.2004.02.010
51. Villiger, M., Bohli, D., Kiper, D., Pyk, P., Spillmann, J., Meilick, B., et al. (2013). Virtual reality-augmented neurorehabilitation improves motor function and reduces neuropathic pain in patients with incomplete spinal cord injury. Neurorehabil. Neural Repair 27, 675-683. doi: 10.1177/1545968313490999
52. Villiger, M., Hepp-Reymond, M. C., Pyk, P., Kiper, D., Spillman, J., Meilick, B., et al. (2011). "Virtual reality rehabilitation system for neuropathic pain and motor dysfunction in spinal cord injury patients," in International Conference on Virtual Rehabilitation (ICVR) (Zurich, Switzerland).
53. Walz, A. D., Doppl, K., Kaza, E., Roschka, S., Platz, T., and Lotze, M. (2015). Changes in cortical, cerebellar and basal ganglia representation after comprehensive long term unilateral hand motor training. Behav. Brain Res. 278, 393-403. doi: 10.1016/j.bbr.2014.08.044
54. Wyndaele, M., and Wyndaele, J. J. (2006). Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord 44, 523-529. doi: 10.1038/sj.sc.3101893
55. Zörner, B., Bachmann, L. C., Filli, L., Kapitza, S., Gullo, M., Bolliger, M., et al. (2014). Chasing central nervous system plasticity: the brainstem's contribution to locomotor recovery in rats with spinal cord injury. Brain 137, 1716-1732. doi: 10.1093/brain/awu078