Long-term sensory stimulation therapy improves hand function and restores cortical responsiveness in patients with chronic cerebral lesions. Three single case studies

Frontiers in Human Neuroscience

Volumn , Issue AUGUST, 2012, Pages

  Kattenstroth, Jan Christoph ^a   Kalisch, Tobias ^a,b   Peters, Sören ^b   Tegenthoff, Martin ^b   Dinse, Hubert R ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Chronic cerebral lesion; Repetitive sensory stimulation; Sensorimotor hand function; Single case

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN DAMAGE; CASE REPORT; CHRONIC DISEASE; CLINICAL ASSESSMENT; CLINICAL EFFECTIVENESS; CLINICAL EVALUATION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION THERAPY; EVOKED CORTICAL RESPONSE; EVOKED SOMATOSENSORY RESPONSE; FEMALE; GRIP STRENGTH; HAND DISEASE; HUMAN; LEFT HANDEDNESS; LONG TERM CARE; MALE; MENTAL PERFORMANCE; MOTOR PERFORMANCE; OUTCOME ASSESSMENT; PARESIS; PERCEPTIVE THRESHOLD; REPEAT PROCEDURE; RESPONSE TIME; RIGHT HANDEDNESS; SENSORIMOTOR FUNCTION; SOMATOSENSORY STIMULATION; STEADY STATE; TACTILE FEEDBACK; THERAPY EFFECT; TOUCH; TREATMENT DURATION;

EID: 84933670984     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00244     Document Type: Article

References (71)

1. Alegria, J., and Bertelson, P. (1970). Time uncertainty, number of alternatives and particular signal-response pair as determinantof choice reaction time. Acta Psychol. 33, 36-44.
2. Biernaskie, J., Szymanska, A., Windle, V., and Corbett, D. (2005). Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur. J. Neurosci. 21, 989-999.
3. Brown, C. E., Aminoltejari, K., Erb, H., Winship, I. R., and Murphy, T. H. (2009). In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J. Neurosci. 29, 1719-1734.
4. Candia, V., Wienbruch, C., Elbert, T., Rockstroh, B., and Ray, W. (2003). Effective behavioral treatment of focal hand dystonia in musicians alters somatosensory cortical organization. Proc. Natl. Acad. Sci. U.S.A. 100, 7942-7946.
5. Celnik, P., Hummel, F., Harris-Love, M., Wolk, R., and Cohen, L. G. (2007). Somatosensory stimulation enhances the effects of training functional hand tasks in patients with chronic stroke. Arch. Phys. Med. Rehabil. 88, 1369-1376.
6. Chen, R., Cohen, L. G., and Hallett, M. (1997). Role of the ipsilateral motor cortex in voluntary movement. Can. J. Neurol. Sci. 24, 284-291.
7. Chen, R., Corwell, B., and Hallett, M. (1999). Modulation of motor cortex excitability by median nerve and digit stimulation. Exp. Brain Res. 129, 77-86.
8. Classen, J., Steinfelder, B., Liepert, J., Stefan, K., Celnik, P., Cohen, L. G., Hess, A., Kunesch, E., Chen, R., Benecke, R., and Hallett, M. (2000). Cutaneomotor integration in humans is somatotopically organized at various levels of the nervous system and is task dependent. Exp. Brain Res. 130, 48-59.
9. Conforto, A. B., Cohen, L. G., dos Santos, R. L., Scaff, M., and Marie, S. K. (2007). Effects of somatosensory stimulation on motor function in chronic cortico-subcortical strokes. J. Neurol. 254, 333-339.
10. Conforto, A. B., Kaelin-Lang, A., and Cohen, L. G. (2002). Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann. Neurol. 51, 122-125.
11. Dinse, H. R. (2006). Cortical reorganization in the aging brain. Prog. Brain Res. 157, 57-80.
12. Dinse, H. R., Boland, J., Kalisch, T., Kraemer, M., Freund, E., Beeser, E., Hömberg, V., and Stephan, K. M. (2008). Repetitive sensory stimulation training in stroke. Eur. J. Neurol. 15(Suppl. 3), 400.
13. Dinse, H. R., Kalisch, T., Ragert, P., Pleger, B., Schwenkreis, P., and Tegenthoff, M. (2005). Improving human haptic performance in normal and impaired human populations through unattended activation-based learning. ACM Trans. Appl. Percept. 2, 71-88.
14. Dinse, H. R., Kattenstroth, J. C., Gattica Tossi, M. A., Tegenthoff, M., and Kalisch, T. (2011). "Sensory stimulation for augmenting perception, sensorimotor behavior and cognition," in Augmenting Cognition eds I. Segev and H. Markram (Lausanne: EPFL Press), 11-39.
15. Dinse, H. R., Kleibel, N., Kalisch, T., Ragert, P., Wilimzig, C., and Tegenthoff, M. (2006). Tactile coac-tivation resets age-related decline of human tactile discrimination. Ann. Neurol. 60, 88-94.
16. Dinse, H. R., Ragert, P., Pleger, B., Schwenkreis, P., and Tegenthoff, M. (2003). Pharmacological modulation of perceptual learning and associated cortical reorganization. Science 301, 91-94.
17. Dobkin, B. H. (2004). Strategies for stroke rehabilitation. Lancet Neurol. 3, 528-536.
18. Ebied, A. M. (2003). The role of cutaneous sensation in the motor function of the hand. J. Orthop. Res. 22, 862-866.
19. Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B., and Taub, E. (1995). Increased cortical representation of the fingers of the left hand in string players. Science 270, 305-307.
20. Folstein, M. F., Folstein, S. E., and McHugh, P. R. (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198.
21. Fraser, C., Power, M., Hamdy, S., Rothwell, J., Hobday, D., Hollander, I., Tyrell, P., Hobson, A., Williams, S., and Thompson, D. (2002). Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 34, 831-840.
22. Gerloff, C., Cohen, L. G., Floeter, M. K., Chen, R., Corwell, B., and Hallett, M. (1998). Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract. J. Physiol. 510(Pt 1), 249-259.
23. Grotta, J. C., Noser, E. A., Ro, T., Boake, C., Levin, H., Aronowski, J., and Schallert, T. (2004). Constraint-induced movement therapy. Stroke 35, 2699-2701.
24. Hackel, M. E., Wolfe, G. A., Bang, S. M., and Canfield, J. S. (1992). Changes in hand function in the aging adult as determined by the Jebsen Test of Hand Function. Phys. Ther. 72, 373-377.
25. Hamdy, S., Rothwell, J. C., Aziz, Q., Singh, K. D., and Thompson, D. G. (1998). Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat. Neurosci. 1, 64-68.
26. Hashimoto, I., Suzuki, A., Kimura, T., Iguchi, Y., Tanosaki, M., Takino, R., Haruta, Y., and Taira, M. (2004). Is there training-dependent reorganization of digit representations in area 3b of string players? Clin. Neurophysiol. 115, 435-447.
27. Jäncke, L., Schlaug, G., and Steinmetz, H. (1997). Hand skill asymmetry in professional musicians. Brain Cogn. 34, 424-432.
28. Jäncke, L., Shah, N. J., and Peters, M. (2000). Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Brain Res. Cogn. Brain Res. 10, 177-183.
29. Jebsen, R. H., Taylor, N., Trieschmann, R. B., Trotter, M. J., and Howard, L. A. (1969). An objective and standardized test of hand function. Arch. Phys. Med. Rehabil. 50, 311-319.
30. Johansson, B. B. (2011). Current trends in stroke rehabilitation. A review with focus on brain plasticity. Acta Neurol. Scand. 123, 147-159.
31. Jones, E. G., Coulter, J. D., and Hendry, S. H. (1978). Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J. Comp. Neurol. 181, 291-347.
32. Kaelin-Lang, A., Luft, A. R., Sawaki, L., Burstein, A. H., Sohn, Y. H., and Cohen, L. G. (2002). Modulation of human corticomotor excitability by somatosensory input. J. Physiol. 540, 623-633.
33. Kalisch, T., Kattenstroth, J. C., Kowalewski, R., Tegenthoff, M., and Dinse, H. R. (2011a). Cognitive and tactile factors affecting human haptic performance in later life. PLoS ONE 7:e30420. doi: 10.1371/journal.pone.0030420
34. Kalisch, T., Richter, R., Lenz, M., Kattenstroth, J. C., Kolankowska, I., Tegenthoff, M., and Dinse, H. R. (2011b). Questionnaire-based evaluation of everyday competence in older adults. Clin. Interv. Aging 6, 37-46.
35. Kalisch, T., Tegenthoff, M., and Dinse, H. (2007). Differential effects of synchronous and asynchronous multifinger coactivation on human tactile performance. BMC Neurosci. 8, 58.
36. Kalisch, T., Tegenthoff, M., and Dinse, H. R. (2008a). Improvement of sensorimotor functions in old age by passive sensory stimulation. Clin. Interv. Aging 3, 673-690.
37. Kalisch, T., Ragert, P., Schwenkreis, P., Dinse, H. R., and Tegenthoff, M. (2008b). Impaired tactile acuity in old age is accompanied by enlarged hand representations in somatosensory cortex. Cereb. Cortex 19, 1530-1538.
38. Kalisch, T., Tegenthoff, M., and Dinse, H. R. (2010). Repetitive electric stimulation elicits enduring improvement of sensorimotor performance in seniors. Neural Plas. 2010, 11.
39. Kalisch, T., Wilimzig, C., Kleibel, N., Tegenthoff, M., and Dinse, H. R. (2006). Age-related attenuation of dominant hand superiority. PLoS ONE 1:e90. doi: 10.1371/journal.pone.0000090
40. Kobayashi, M., Ng, J., Théoret, H., and Pascual-Leone, A. (2003). Modulation of intracortical neu-ronal circuits in human hand motor area by digit stimulation. Exp. Brain Res. 149, 1-8.
41. Kowalewski, R., Kattenstroth, J. C., Kalisch, T., and Dinse, H. R. (2012). Improved acuity and dexterity but unchanged touch and pain thresholds following repetitive sensory stimulation of the fingers. Neural Plast. 2012, 974504.
42. Krakauer, J. W. (2006). Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr. Opin. Neurol. 19, 84-90.
43. Lederman, S. J., and Klatzky, R. L. (2004). Haptic identification of common objects: effects of constraining the manual exploration process. Percept. Psychophys. 66, 618-628.
44. Lenz, M., Tegenthoff, M., Kohlhaas, K., Stude, P., Höffken, O., Tossi, M., Kalisch, T., and Dinse, H. (2012). Increased excitability of somatosen-sory cortex in aged humans is associated with impaired tactile acuity. J. Neurosci. 32, 1811-1816.
45. Liepert, J., Hamzei, F., and Weiller, C. (2000). Motor cortex disinhibi-tion of the unaffected hemisphere after acute stroke. Muscle Nerve 23, 1761-1763.
46. Liepert, J., Uhde, I., Gräf, S., Leidner, O., and Weiller, C. (2001). Motor cortex plasticity during forced-use therapy in stroke patients: a preliminary study. J. Neurol. 248, 315-321.
47. Lincoln, N., and Leadbitter, D. (1979). Assessment of motor function in stroke patients. Physiotherapy 65, 48-51.
48. McDonnell, M. N., and Ridding, M. C. (2006). Afferent stimulation facilitates performance on a novel motor task. Exp. Brain Res. 170, 109-115.
49. Montoya, P., and Sitges, C. (2006). Affective modulation of somatosensory-evoked potentials elicited by tactile stimulation. Brain Res. 1068, 205-212.
50. Murphy, T. H., and Corbett, D. (2009). Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci. 10, 861-872.
51. Nudo, R. J., Wise, B. M., SiFuentes, F., and Milliken, G. W. (1996). Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272, 1791-1794.
52. Pavlides, C., Miyashita, E., and Asanuma, H. (1993). Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. J. Neurophysiol. 70, 733-741.
53. Pleger, B., Dinse, H. R., Ragert, P., Schwenkreis, P., Malin, J. P., and Tegenthoff, M. (2001). Shifts in cortical representations predict human discrimination improvement. Proc. Natl. Acad. Sci. U.S.A. 98, 12255-12260.
54. Pleger, B., Foerster, A. F., Ragert, P., Dinse, H. R., Schwenkreis, P., Malin, J. P., Nicolas, V., and Tegenthoff, M. (2003). Functional imaging of perceptual learning in human primary and secondary somatosensory cortex. Neuron 40, 643-653.
55. Ragert, P., Franzkowiak, S., Schwenkreis, P., Tegenthoff, M., and Dinse, H. R. (2008). Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex. Exp. Brain Res. 184, 1-11.
56. Raven, J. C. (1938). Progressive Matrices. London: Lewis and Co.
57. Ridding, M. C., and Uy, J. (2003). Changes in motor cortical excitability induced by paired associative stimulation. Clin. Neurophysiol. 114, 1437-1444.
58. Ridding, M. C., Brouwer, B., Miles, T. S., Pitcher, J. B., and Thompson, P. D. (2000). Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp. Brain Res. 131, 135-143.
59. Ridding, M. C., McKay, D. R., Thompson, P. D., and Miles, T. S. (2001). Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin. Neurophysiol. 112, 1461-1469.
60. Smith, P., Dinse, H., Kalisch, T., Johnson, M., and Walker-Batson, D. (2009). Effects of repetitive electrical stimulation to treat sensory loss in persons poststroke. Arch. Phys. Med. Rehabil. 90, 2108-2111.
61. Steingrueber, H. J. (1971). Zur mes-sung der haendigkeit. Zeitschrift fuer Experimentelle und Angewandte Psychologie 18, 337-357.
62. Stepniewska, I., Preuss, T. M., and Kaas, J. H. (1993). Architectonics, soma-totopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J. Comp. Neurol. 330, 238-271.
63. Taub, E., Uswatte, G., and Elbert, T. (2002). New treatments in neurorehabilitation founded on basic research. Nat. Rev. Neurosci. 3, 228-236.
64. Taub, E., Uswatte, G., and Pidikiti, R. (1999). Constraint-induced movement therapy: a new family of techniques with broad application to physical rehabilitation-a clinical review. J. Rehabil. Res. Dev. 36, 237-251.
65. Webster, B. R., Celnik, P. A., and Cohen, L. G. (2006). Noninvasive brain stimulation in stroke rehabilitation. NeuroRx 3, 474-481.
66. Wienbruch, C., Candia, V., Svensson, J., Kleiser, R., and Kollias, S. S. (2006). A portable and low-cost fMRI compatible pneumatic system for the investigation of the somatosensen-sory system in clinical and research environments. Neurosci. Lett. 398, 183-188.
67. Wilimzig, C., Ragert, P., and Dinse, H. R. (2012). Cortical topography of intracortical inhibition influences the speed of decision making. Proc. Natl. Acad. Sci. U.S.A. 109, 3107-3112.
68. Woldag, H., Waldmann, G., Heuschkel, G., and Hummelsheim, H. (2003). Is the repetitive training of complex hand and arm movements beneficial for motor recovery in stroke patients? Clin. Rehabil. 17, 723-730.
69. Wu, C. W., and Kaas, J. H. (2003). Somatosensory cortex of prosimian Galagos: physiological recording, cytoarchitecture, and corticocorti-cal connections of anterior parietal cortex and cortex of the lateral sul-cus. J. Comp. Neurol. 457, 263-292.
70. Wu, C. W., Seo, H. J., and Cohen, L. G. (2006). Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke. Arch. Phys. Med. Rehabil. 87, 351-357.
71. Zhan, S., and Ottenbacher, K. J. (2001). Single subject research designs for disability research. Disabil. Rehabil. 23, 1-8