Brain motor functional changes after somatosensory discrimination training

Abstract

Somatosensory discrimination training may modulate cognitive processes, such as movement planning and monitoring, which can be useful during active movements. The aim of the study was to assess the effect of somatosensory discrimination training on brain functional activity using functional magnetic resonance imaging (fMRI) during motor and sensory tasks in healthy subjects. Thirty-nine healthy young subjects were randomized into two groups: the experimental group underwent somatosensory discrimination training consisting of shape, surface and two-point distance discrimination; and the control group performed a simple object manipulation. At baseline and after 2 weeks of training, subjects underwent sensorimotor evaluations and fMRI tasks consisting of right-hand tactile stimulation, manipulation of a simple object, and complex right-hand motor sequence execution. Right-hand dexterity improved in both groups, but only the experimental group showed improvements in all manual dexterity tests. After training, the experimental group showed: decreased activation of the ipsilateral sensorimotor areas during the tactile stimulation task; increased activation of the contralateral postcentral gyrus and thalamus bilaterally during the manipulation task; and a reduced recruitment of the ipsilateral pre/postcentral gyri and an increased activation of the basal ganglia and cerebellum contralaterally during the complex right-hand motor task. In healthy subjects, sensory discrimination training was associated with lateralization of brain activity in sensorimotor areas during sensory and motor tasks. Further studies are needed to investigate the usefulness of this training in motor rehabilitation of patients with focal lesions in the central nervous system.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aman, J. E., Elangovan, N., Yeh, I. L., & Konczak, J. (2014). The effectiveness of proprioceptive training for improving motor function: a systematic review. Frontiers in Human Neuroscience, 8, 1075.

    PubMed  Google Scholar 

  2. Binkofski, F., Buccino, G., Posse, S., Seitz, R. J., Rizzolatti, G., & Freund, H. (1999). A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. The European Journal of Neuroscience, 11(9), 3276–3286.

    Article  PubMed  CAS  Google Scholar 

  3. Borich, M. R., Brodie, S. M., Gray, W. A., Ionta, S., & Boyd, L. A. (2015). Understanding the role of the primary somatosensory cortex: opportunities for rehabilitation. Neuropsychologia, 79(Pt B), 246–255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Butefisch, C. M., Wessling, M., Netz, J., Seitz, R. J., & Homberg, V. (2008). Relationship between interhemispheric inhibition and motor cortex excitability in subacute stroke patients. Neurorehabilitation and Neural Repair, 22(1), 4–21.

    Article  PubMed  Google Scholar 

  5. Carel, C., Loubinoux, I., Boulanouar, K., Manelfe, C., Rascol, O., Celsis, P., et al. (2000). Neural substrate for the effects of passive training on sensorimotor cortical representation: a study with functional magnetic resonance imaging in healthy subjects. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism, 20(3), 478–484.

    Article  CAS  Google Scholar 

  6. Carey, L. M., & Matyas, T. A. (2005). Training of somatosensory discrimination after stroke: facilitation of stimulus generalization. American Journal of Physical Medicine & Rehabilitation / Association of Academic Physiatrists, 84(6), 428–442.

    Article  Google Scholar 

  7. Carey, L. M., Matyas, T. A., & Oke, L. E. (1993). Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. Archives of Physical Medicine and Rehabilitation, 74(6), 602–611.

    Article  PubMed  CAS  Google Scholar 

  8. Chen, J. C., Lin, C. H., Wei, Y. C., Hsiao, J., & Liang, C. C. (2011). Facilitation of motor and balance recovery by thermal intervention for the paretic lower limb of acute stroke: a single-blind randomized clinical trial. Clinical Rehabilitation, 25(9), 823–832.

    Article  PubMed  Google Scholar 

  9. Cordo, P., Lutsep, H., Cordo, L., Wright, W. G., Cacciatore, T., & Skoss, R. (2009). Assisted movement with enhanced sensation (AMES): coupling motor and sensory to remediate motor deficits in chronic stroke patients. Neurorehabilitation and Neural Repair, 23(1), 67–77.

    Article  PubMed  Google Scholar 

  10. Cramer, S. C. (2008). Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Annals of Neurology, 63(3), 272–287.

    Article  PubMed  Google Scholar 

  11. Ebersbach, G., Edler, D., Kaufhold, O., & Wissel, J. (2008). Whole body vibration versus conventional physiotherapy to improve balance and gait in Parkinson’s disease. Archives of Physical Medicine and Rehabilitation, 89(3), 399–403.

    Article  PubMed  Google Scholar 

  12. Gotts, S. J., Jo, H. J., Wallace, G. L., Saad, Z. S., Cox, R. W., & Martin, A. (2013). Two distinct forms of functional lateralization in the human brain. Proceedings of the National Academy of Sciences of the United States of America, 110(36), E3435–E3444.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hamdy, S., Rothwell, J. C., Aziz, Q., Singh, K. D., & Thompson, D. G. (1998). Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nature Neuroscience, 1(1), 64–68.

    Article  PubMed  CAS  Google Scholar 

  14. Herrero, M. T., Barcia, C., & Navarro, J. M. (2002). Functional anatomy of thalamus and basal ganglia. Child’s Nervous System: ChNS: Official Journal of the International Society for Pediatric Neurosurgery, 18(8), 386–404.

    Article  Google Scholar 

  15. Hodics, T., Cohen, L. G., & Cramer, S. C. (2006). Functional imaging of intervention effects in stroke motor rehabilitation. Archives of Physical Medicine and Rehabilitation, 87(12 Suppl 2), S36-42.

    PubMed  Google Scholar 

  16. Hubbard, I. J., Carey, L. M., Budd, T. W., Levi, C., McElduff, P., Hudson, S., et al. (2015). A randomized controlled trial of the effect of early upper-limb training on stroke recovery and brain activation. Neurorehabilitation and Neural Repair, 29(8), 703–713.

    Article  PubMed  Google Scholar 

  17. Jouen, A. L., Verwey, W. B., van der Helden, J., Scheiber, C., Neveu, R., Dominey, P. F., et al. (2013). Discrete sequence production with and without a pause: the role of cortex, basal ganglia, and cerebellum. Frontiers in Human Neuroscience, 7, 492.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kato, H., & Izumiyama, M. (2015). Impaired motor control due to proprioceptive sensory loss in a patient with cerebral infarction localized to the postcentral gyrus. Journal of Rehabilitation Medicine, 47(2), 187–190.

    Article  PubMed  Google Scholar 

  19. Kelly, A. M., & Garavan, H. (2005). Human functional neuroimaging of brain changes associated with practice. Cerebral Cortex, 15(8), 1089–1102.

    Article  PubMed  Google Scholar 

  20. Lee, M. Y., Park, J. W., Park, R. J., Hong, J. H., Son, S. M., Ahn, S. H., et al. (2009). Cortical activation pattern of compensatory movement in stroke patients. NeuroRehabilitation, 25(4), 255–260.

    PubMed  Google Scholar 

  21. Luo, C., Zhang, X., Cao, X., Gan, Y., Li, T., Cheng, Y., et al. (2016). The lateralization of intrinsic networks in the aging brain implicates the effects of cognitive training. Frontiers in Aging Neuroscience, 8, 32.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lustig, C., Shah, P., Seidler, R., & Reuter-Lorenz, P. A. (2009). Aging, training, and the brain: a review and future directions. Neuropsychology Review, 19(4), 504–522.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lynch, E. A., Hillier, S. L., Stiller, K., Campanella, R. R., & Fisher, P. H. (2007). Sensory retraining of the lower limb after acute stroke: a randomized controlled pilot trial. Archives of Physical Medicine and Rehabilitation, 88(9), 1101–1107.

    Article  PubMed  Google Scholar 

  24. Mace, M. J., Levin, O., Alaerts, K., Rothwell, J. C., & Swinnen, S. P. (2008). Corticospinal facilitation following prolonged proprioceptive stimulation by means of passive wrist movement. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society, 25(4), 202–209.

    Article  Google Scholar 

  25. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19(3), 1233–1239.

    Article  PubMed  Google Scholar 

  26. Manganotti, P., Patuzzo, S., Cortese, F., Palermo, A., Smania, N., & Fiaschi, A. (2002). Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology, 113(6), 936–943.

    Article  CAS  Google Scholar 

  27. Mathiowetz, V., Kashman, N., Volland, G., Weber, K., Dowe, M., & Rogers, S. (1985). Grip and pinch strength: normative data for adults. Archives of Physical Medicine and Rehabilitation, 66(2), 69–74.

    PubMed  CAS  Google Scholar 

  28. Matyas, F., Sreenivasan, V., Marbach, F., Wacongne, C., Barsy, B., Mateo, C., et al. (2010). Motor control by sensory cortex. Science, 330(6008), 1240–1243.

    Article  PubMed  CAS  Google Scholar 

  29. Merkert, J., Butz, S., Nieczaj, R., Steinhagen-Thiessen, E., & Eckardt, R. (2011). Combined whole body vibration and balance training using Vibrosphere(R): improvement of trunk stability, muscle tone, and postural control in stroke patients during early geriatric rehabilitation. Zeitschrift fur Gerontologie und Geriatrie, 44(4), 256–261.

    Article  PubMed  CAS  Google Scholar 

  30. Mezzapesa, D. M., Rocca, M. A., Rodegher, M., Comi, G., & Filippi, M. (2008). Functional cortical changes of the sensorimotor network are associated with clinical recovery in multiple sclerosis. Human Brain Mapping, 29(5), 562–573.

    Article  PubMed  Google Scholar 

  31. Nakamura, K., Sakai, K., & Hikosaka, O. (1998). Neuronal activity in medial frontal cortex during learning of sequential procedures. Journal of Neurophysiology, 80(5), 2671–2687.

    Article  PubMed  CAS  Google Scholar 

  32. Nolan, M. F. (1982). Two-point discrimination assessment in the upper limb in young adult men and women. Physical Therapy, 62(7), 965–969.

    Article  PubMed  CAS  Google Scholar 

  33. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.

    Article  PubMed  CAS  Google Scholar 

  34. Rao, S. M., Binder, J. R., Bandettini, P. A., Hammeke, T. A., Yetkin, F. Z., Jesmanowicz, A., et al. (1993). Functional magnetic resonance imaging of complex human movements. Neurology, 43(11), 2311–2318.

    Article  PubMed  CAS  Google Scholar 

  35. Rosenkranz, K., Butler, K., Williamon, A., & Rothwell, J. C. (2009). Regaining motor control in musician’s dystonia by restoring sensorimotor organization. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(46), 14627–14636.

    Article  CAS  Google Scholar 

  36. Rosenkranz, K., & Rothwell, J. C. (2012). Modulation of proprioceptive integration in the motor cortex shapes human motor learning. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 32(26), 9000–9006.

    Article  CAS  Google Scholar 

  37. Savini, N., Babiloni, C., Brunetti, M., Caulo, M., Del Gratta, C., Perrucci, M. G., et al. (2010). Passive tactile recognition of geometrical shape in humans: an fMRI study. Brain Research Bulletin, 83(5), 223–231.

    Article  PubMed  Google Scholar 

  38. Shimizu, T., Hosaki, A., Hino, T., Sato, M., Komori, T., Hirai, S., et al. (2002). Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain: A Journal of Neurology, 125(Pt 8), 1896–1907.

    Article  Google Scholar 

  39. Shimoyama, I., Ninchoji, T., & Uemura, K. (1990). The finger-tapping test. A quantitative analysis. Archives of Neurology, 47(6), 681–684.

    Article  PubMed  CAS  Google Scholar 

  40. Sirigu, A., Duhamel, J. R., Cohen, L., Pillon, B., Dubois, B., & Agid, Y. (1996). The mental representation of hand movements after parietal cortex damage. Science, 273(5281), 1564–1568.

    Article  PubMed  CAS  Google Scholar 

  41. Stoeckel, M. C., Weder, B., Binkofski, F., Buccino, G., Shah, N. J., & Seitz, R. J. (2003). A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study. NeuroImage, 19(3), 1103–1114.

    Article  PubMed  Google Scholar 

  42. Struppler, A., Havel, P., & Muller-Barna, P. (2003). Facilitation of skilled finger movements by repetitive peripheral magnetic stimulation (RPMS)—a new approach in central paresis. NeuroRehabilitation, 18(1), 69–82.

    PubMed  CAS  Google Scholar 

  43. Surrey, L. R., Nelson, K., Delelio, C., Mathie-Majors, D., Omel-Edwards, N., Shumaker, J., et al. (2003). A comparison of performance outcomes between the Minnesota rate of manipulation test and the Minnesota manual dexterity test. Work, 20(2), 97–102.

    PubMed  Google Scholar 

  44. Tesio, L., Simone, A., Zebellin, G., Rota, V., Malfitano, C., & Perucca, L. (2016). Bimanual dexterity assessment: validation of a revised form of the turning subtest from the Minnesota dexterity test. International Journal of Rehabilitation Research. Internationale Zeitschrift fur Rehabilitationsforschung. Revue Internationale de Recherches de Readaptation, 39(1), 57–62.

    Article  PubMed  Google Scholar 

  45. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.

    Article  PubMed  CAS  Google Scholar 

  46. Vahdat, S., Darainy, M., & Ostry, D. J. (2014). Structure of plasticity in human sensory and motor networks due to perceptual learning. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34(7), 2451–2463.

    Article  CAS  Google Scholar 

  47. van Nes, I. J., Geurts, A. C., Hendricks, H. T., & Duysens, J. (2004). Short-term effects of whole-body vibration on postural control in unilateral chronic stroke patients: preliminary evidence. American Journal of Physical Medicine & Rehabilitation / Association of Academic Physiatrists, 83(11), 867–873.

    Article  Google Scholar 

  48. van Nes, I. J., Latour, H., Schils, F., Meijer, R., van Kuijk, A., & Geurts, A. C. (2006). Long-term effects of 6-week whole-body vibration on balance recovery and activities of daily living in the postacute phase of stroke: a randomized, controlled trial. Stroke; A Journal of Cerebral Circulation, 37(9), 2331–2335.

    Article  Google Scholar 

  49. Ward, N. S., Brown, M. M., Thompson, A. J., & Frackowiak, R. S. (2003a). Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain: A Journal of Neurology, 126(Pt 11), 2476–2496.

    Article  CAS  Google Scholar 

  50. Ward, N. S., Brown, M. M., Thompson, A. J., & Frackowiak, R. S. (2003b). Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain: A Journal of Neurology, 126(Pt 6), 1430–1448.

    Article  CAS  Google Scholar 

  51. Wolpert, D. M., & Ghahramani, Z. (2000). Computational principles of movement neuroscience. Nature Neuroscience, (3 Suppl), 1212–1217.

  52. Wong, J. D., Kistemaker, D. A., Chin, A., & Gribble, P. L. (2012). Can proprioceptive training improve motor learning? Journal of Neurophysiology, 108(12), 3313–3321.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Worsley, K. J., & Friston, K. J. (1995). Analysis of fMRI time-series revisited–again. NeuroImage, 2(3), 173–181.

    Article  PubMed  CAS  Google Scholar 

  54. Yozbatiran, N., Donmez, B., Kayak, N., & Bozan, O. (2006). Electrical stimulation of wrist and fingers for sensory and functional recovery in acute hemiplegia. Clinical Rehabilitation, 20(1), 4–11.

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Massimo Filippi.

Ethics declarations

Funding

None.

Conflict of interest

E. Sarasso, F. Temporiti, P. Adamo, F. Piccolo, R. Gatti report no disclosures.

F. Agosta is Section Editor of NeuroImage: Clinical; has received speaker honoraria from ExceMED – Excellence in Medical Education and Biogen Idec; and receives or has received research supports from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA), and the European Research Council.

M. Copetti has received compensation for consulting and/or serving on advisory boards from Teva Pharmaceuticals and Biogen Idec.

M. Filippi is Editor-in-Chief of the Journal of Neurology; serves on a scientific advisory board for Teva Pharmaceutical Industries; has received compensation for consulting services and/or speaking activities from Biogen Idec, ExceMED, Novartis, and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Teva Pharmaceutical Industries, Novartis, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, Cure PSP, Alzheimer’s Drug Discovery Foundation (ADDF), the Jacques and Gloria Gossweiler Foundation (Switzerland), and ARiSLA (Fondazione Italiana di Ricerca per la SLA).

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sarasso, E., Agosta, F., Temporiti, F. et al. Brain motor functional changes after somatosensory discrimination training. Brain Imaging and Behavior 12, 1011–1021 (2018). https://doi.org/10.1007/s11682-017-9763-2

Download citation

Keywords

  • Functional magnetic resonance imaging
  • Healthy volunteers
  • Sensorimotor cortex
  • Touch perception
  • Physical therapy