Advertisement

European Radiology

, Volume 15, Issue 9, pp 1806–1814 | Cite as

Functional MRI activation of somatosensory and motor cortices in a hand-grafted patient with early clinical sensorimotor recovery

  • C. Neugroschl
  • V. Denolin
  • F. Schuind
  • C. Van Holder
  • P. David
  • D. Balériaux
  • T Metens
Neuro

Abstract

The aim of this study was to investigate somatosensory and motor cortical activity with functional MRI (fMRI) in a hand-grafted patient with early clinical recovery. The patient had motor fMRI examinations before transplantation, and motor and passive tactile stimulations after surgery. His normal hand and a normal group were studied for comparison. A patient with complete brachial plexus palsy was studied to assess the lack of a fMRI signal in somatosensory areas in the case of total axonal disconnection. Stimulating the grafted hand revealed significant activation in the contralateral somatosensory cortical areas in all fMRI examinations. The activation was seen as early as 10 days after surgery; this effect cannot be explained by the known physiological mechanisms of nerve regeneration. Although an imagination effect cannot be excluded, the objective clinical recovery of sensory function led us to formulate the hypothesis that a connection to the somatosensory cortex was rapidly established. Additional cases and fundamental studies are needed to assess this hypothesis, but several observations were compatible with this explanation. Before surgery, imaginary motion of the amputated hand produced less intense responses than executed movements of the intact hand, whereas the normal activation pattern for right-handed subjects was found after surgery, in agreement with the good clinical motor recovery.

Keywords

Functional magnetic resonance imaging Somatosensory cortex Hand transplantation 

References

  1. 1.
    Jensen JN, Mackinnon SE (2000) Composite tissue allotransplantation: a comprehensive review of the literature—part III. J Reconstr Microsurg 16(3):235–251Google Scholar
  2. 2.
    Graham B, Adkins P, Tsai TM, Firrell J, Breidenbach WC (1998) Major replantation versus revision amputation and prosthetic fitting in the upper extremity: a late functional outcomes study. J Hand Surg (Am) 23(5):783–791Google Scholar
  3. 3.
    Petit F, Minns AB, Dubernard JM, Hettiaratchy S, Lee WP (2003) Composite tissue allotransplantation and reconstructive surgery: first clinical applications. Ann Surg 237(1):19–25Google Scholar
  4. 4.
    Dubernard JM, Owen E, Lefrancois N, Petruzzo P, Martin X, Dawahra M, Jullien D, Kanitakis J, Frances C, Preville X, Gebuhrer L, Hakim N, Lanzetta M, Kapila H, Herzberg G, Revillard JP (2000) First human hand transplantation. Case report. Transpl Int 13(Suppl 1):S521–S524Google Scholar
  5. 5.
    Jones NF (2002) Concerns about human hand transplantation in the 21st century. J Hand Surg (Am) 27(5):771–787Google Scholar
  6. 6.
    Francois CG, Breidenbach WC, Maldonado C, Kakoulidis TP, Hodges A, Dubernard JM, Owen E, Pei G, Ren X, Barker JH (2000) Hand transplantation: comparisons and observations of the first four clinical cases. Microsurgery 20(8):360–371Google Scholar
  7. 7.
    Lotze M, Flor H, Grodd W, Larbig W, Birbaumer N (2001) Phantom movements and pain. An fMRI study in upper limb amputees. Brain 124:2268–2277Google Scholar
  8. 8.
    Giraux P, Sirigu A, Scheiderandt F, Dubernard JM (2001) Cortical reorganization in motor cortex after graft of both hands. Nat Neurosci 4:691–692Google Scholar
  9. 9.
    Torquati K, Pizzella V, Della Penna S, Franciotti R, Babiloni C, Romani GL, Rossini PM (2003) “Gating” effects of simultaneous peripheral electrical stimulations on human secondary somatosensory cortex: a whole-head MEG study. NeuroImage 20(3):1704–1713Google Scholar
  10. 10.
    Hoechstetter K, Rupp A, Stancak A, Meinck HM, Stippich C, Berg P, Scherg M (2001) Interaction of tactile input in the human primary and secondary somatosensory cortex—a magnetoencephalographic study. NeuroImage 14(3):759–767Google Scholar
  11. 11.
    Burton H, Videen TO, Raichle ME (1993) Tactile-vibration-activated foci in insular and parietal–opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. Somatosens Motor Res 10(3):297–308Google Scholar
  12. 12.
    Dettmers C, Connelly A, Stephan K, Turner R, Friston K, Frackowiak R, Gadian D (1996) Quantitative comparison of functional magnetic resonance imaging with positron emission tomography using a force-related paradigm. NeuroImage 4(3 Pt 1):201–209Google Scholar
  13. 13.
    Hagen MC, Pardo JV (2002) PET studies of somatosensory processing of light touch. Behav Brain Res 135(1–2):133–140Google Scholar
  14. 14.
    Gelnar PA, Krauss BR, Szeveren NM, Apkarian AV (1998) Fingertip representation in the human somatosensory cortex: an fMRI study. NeuroImage 7:261–283Google Scholar
  15. 15.
    Sakai K, Watanabe E, Ondera Y, Itagaki H, Yamamotot E, Koizumi H, Miyahita Y (1995) Functional mapping of the human somatosensory cortex with echo-planar MRI. Magn Reson Med 33:736–743Google Scholar
  16. 16.
    Moore CI, Stern C, Corkin S, Gray A, Thelusma F, Rosen B, Dale A (1997) Segregation of multiple somatosensory maps within the human postcentral gyrus using fMRI. NeuroImage S406Google Scholar
  17. 17.
    Harrington G, Raman M, Kussel N, Downs III J (1998) Somatosensory response to vibrotactile stimuli in fMRI. NeuroImage S401Google Scholar
  18. 18.
    McGonigle D, Aston P, Joseph O, Frackowiak R (1998) Somatotopy of vibrotactile stimulation in SI: an fMRI study. NeuroImage S405Google Scholar
  19. 19.
    Ferretti A, Babiloni C, Gratta CD, Caulo M, Tartaro A, Bonomo L, Rossini PM, Romani GL (2003) Functional topography of the secondary somatosensory cortex for nonpainful and painful stimuli: an fMRI study. NeuroImage 20(3):1625–1638Google Scholar
  20. 20.
    Simoes C, Mertens M, Forss N, Jousmaki V, Lutkenhoner B, Hari R (2001) Functional overlap of finger representations in human SI and SII cortices J Neurophysiol 86(4):1661–1665Google Scholar
  21. 21.
    Wegner K, Forss N, Salenius S (2000) Characteristics of the human contra-versus ipsilateral SII cortex. Clin Neurophysiol 111(5):894–900Google Scholar
  22. 22.
    Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113Google Scholar
  23. 23.
    Whitsel BL, Petrucelli LM, Werner G (1969) Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. J Neurophysiol 32(2):170–183Google Scholar
  24. 24.
    Friston KJ, Ashburner L, Frith CD, Poline JB, Hether JD, Frackowiak RS (1995) Spatial registration and normalization of images. Hum Brain Mapp 3:165–189Google Scholar
  25. 25.
    Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, StuttgartGoogle Scholar
  26. 26.
    Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210Google Scholar
  27. 27.
    Friston KJ, Holmes AP, Worsley KJ (1999) How many subjects constitute a study? NeuroImage 10:1–5Google Scholar
  28. 28.
    Gelnar PA, Krauss BR, Sheehe PR, Szeverenyi NM, Apkarian AV (1999) A comparative fMRI study of cortical representations for thermal painful, vibrotactile, and motor performance tasks. NeuroImage 10(4):460–482Google Scholar
  29. 29.
    Polonara G, Fabri M, Manzoni T, Salvolini U (1999) Localization of the first and second somatosensory areas in the human cerebral cortex with functional MR imaging. Am J Neuroradiol 20(2):199–205Google Scholar
  30. 30.
    Hansson T, Brismar P (1999) Tactile stimulation of the hand causes bilateral cortical activation: a functional magnetic resonance study in humans. Neurosci Lett 271:29–32Google Scholar
  31. 31.
    Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RS (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84(2):393–402Google Scholar
  32. 32.
    Grafton ST, Woods RP, Mazziotta JC (1993) Within-arm somatotopy in human motor areas determined by positron emission tomography imaging of cerebral blood flow. Exp Brain Res 95(1):172–176Google Scholar
  33. 33.
    Murray EA, Mishkin M (1984) Relative contributions of SII and area 5 to tactile discrimination in monkeys. Behav Brain Res 11(1):67–83Google Scholar
  34. 34.
    Yahagi S, Kasai T (1999) Motor evoked potentials induced by motor imagery reveal a functional asymmetry of cortical motor control in left- and right-handed human subjects. Neurosci Lett 276(3):185–188Google Scholar
  35. 35.
    Triggs WJ, Calvanio R, Levine M (1997) Transcranial magnetic stimulation reveals a hemispheric asymmetry correlate of intermanual differences in motor performance. Neuropsychologia 35(10):1355–1363Google Scholar
  36. 36.
    Mackinnon SE, Hudson AR, Bojanowski V, Hunter DA, Maraghi E (1985) Peripheral nerve injection injury with purified bovine collagen—an experimental model in the rat. Ann Plast Surg 14(5):428–436Google Scholar
  37. 37.
    Bain JR (2000) Peripheral nerve and neuromuscular allotransplantation: current status. Microsurgery 20:384–388Google Scholar
  38. 38.
    Wang MS, Gold BG (1999) FK506 increases the regeneration of spinal cord axons in a predegenerated peripheral nerve autograft. J Spinal Cord Med 22(4):287–296Google Scholar
  39. 39.
    Doolabh VB, Mackinnon SE (1999) FK506 accelerates functional recovery following nerve grafting in a rat model. Plast Reconstr Surg 103(7):1928–1936Google Scholar
  40. 40.
    Golaszewski SM, Siedentopf CM, Baldauf E, Koppelstaetter F et al (2002) Functional magnetic resonance imaging of the human sensorimotor cortex using a novel vibrotactile stimulator. NeuroImage 17(1):421–430Google Scholar
  41. 41.
    Francis ST, Kelly EF, Bowtell R et al (2000) FMRI of the responses to vibratory stimulation of digit tips. NeuroImage 11:188–202Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • C. Neugroschl
    • 1
  • V. Denolin
    • 1
  • F. Schuind
    • 1
  • C. Van Holder
    • 1
  • P. David
    • 1
  • D. Balériaux
    • 1
  • T Metens
    • 1
  1. 1.ULB-Hopital Erasme, RadiologyBrusselsBelgium

Personalised recommendations