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Experimental Brain Research

, Volume 210, Issue 1, pp 1–11 | Cite as

Stump nerve signals during transcranial magnetic motor cortex stimulation recorded in an amputee via longitudinal intrafascicular electrodes

  • P. M. Rossini
  • Jacopo Rigosa
  • Silvestro Micera
  • Giovanni Assenza
  • Luca Rossini
  • Florinda Ferreri
Research Article

Abstract

Do central and peripheral motor pathways associated with an amputated limb retain at least some functions over periods of years? This problem could be addressed by evaluating the response patterns of nerve signals from peripheral motor fibers during transcranial magnetic stimulation (TMS) of corticospinal tracts. The aim of this study was to record for the first time TMS-related responses from the nerves of a left arm stump of an amputee via intrafascicular longitudinal flexible multi-electrodes (tfLIFE4) implanted for a prosthetic hand control. After tfLIFE4 implant in the stump median and ulnar nerves, TMS impulses of increasing intensity were delivered to the contralateral motor cortex while tfLIFE4 recordings were carried out. Combining TMS of increasing intensity and tfLIFE4 electrodes recordings, motor nerve activity possibly related to the missing limb motor control and selectively triggered by brain stimulation without significant electromyographic contamination was identified. These findings are entirely original and indicate that tfLIFE4 signals are clearly driven from M1 stimulation, therefore witnessing the presence in the stump nerves of viable motor signals from the CNS possibly useful for artificial prosthesis control.

Keywords

Transcranial magnetic stimulation Intrafascicular longitudinal flexible multi-electrodes Peripheral nerves signals 

Notes

Acknowledgments

The research was granted by University Campus Biomedico of Rome, Italy, Scuola Superiore Sant’Anna of Pisa, Italy.

References

  1. Amassian VE, Cracco RQ (1987) Human cerebral cortical responses to contralateral transcranial stimulation. Neurosurg 20(1):148–155Google Scholar
  2. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107 No abstract availablePubMedCrossRefGoogle Scholar
  3. Bennett KM, Lemon RN (1994) The influence of single monkey cortico-motoneuronal cells at different levels of activity in target muscles. J Physiol 477(Pt 2):291–307PubMedGoogle Scholar
  4. Burke D, Hicks R, Gandevia SC, Stephen J, Woodforth I, Crawford M (1993) Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol 470:383–393. Erratum in: J Physiol (Lond) 1994 May 1;476(3):553Google Scholar
  5. Calford MB (2002) Dynamic representational plasticity in sensory cortex. Neuroscience 111(4):709–738 ReviewPubMedCrossRefGoogle Scholar
  6. Caramia MD, Pardal AM, Zarola F, Rossini PM (1989) Electric vs magnetic trans-cranial stimulation of the brain in healthy humans: a comparative study of central motor tracts ‘conductivity’ and ‘excitability’. Brain Res 479(1):98–104PubMedCrossRefGoogle Scholar
  7. Chang WC, Kliot M, Sretavan DW (2008) Microtechnology and nanotechnology in nerve repair. Neurol Res 30(10):1053–1062 ReviewPubMedCrossRefGoogle Scholar
  8. Citi L, Carpaneto J, Yoshida K, Hoffmann KP, Koch KP, Dario P, Micera S (2008) On the use of wavelet denoising and spike sorting techniques to process electroneurographic signals recorded using intraneural electrodes. J Neurosci Methods 172(2):294–302PubMedCrossRefGoogle Scholar
  9. Cohen LG, Bandinelli S, Findley TW, Hallett M (1991) Motor reorganization after upper limb amputation in man :a study with focal magnetic stimulation. Brain 114(Pt 1B):615–627PubMedCrossRefGoogle Scholar
  10. Cowan JM, Day BL, Marsden C, Rothwell JC (1986) The effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man. J Physiol 377:333–347PubMedGoogle Scholar
  11. Deschênes M, Labelle A, Landry P (1979) Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Res 178(2–3):251–274PubMedCrossRefGoogle Scholar
  12. Dhillon GS, Lawrence SM, Hutchinson DT, Horch KW (2004) Residual function in peripheral nerve stumps of amputees: implications for neural control of artificial limbs. J Hand Surg Am 29:605–615; discussion 616–608Google Scholar
  13. Dhillon GS, Kruger TB, Sandhu JS, Horch KW (2005) Effects of short-term training on sensory and motor function in severed nerves of long-term human amputees. J Neurophysiol 93:2625–2633PubMedCrossRefGoogle Scholar
  14. Di Lazzaro V, Oliviero A, Profice P, Meglio M, Cioni B, Tonali P, Rothwell JC (2001) Descending spinal cord volleys evoked by transcranial magnetic and electrical stimulation of the motor cortex leg area in conscious humans. J Physiol 537(Pt 3):1047–1058PubMedGoogle Scholar
  15. Edgley SA, Eyre JA, Lemon RN, Miller S (1990) Excitation of the corticospinal tract by electromagnetic and electrical stimulation of the scalp in the macaque monkey. J Physiol 425:301–320PubMedGoogle Scholar
  16. Edgley SA, Eyre JA, Lemon RN, Miller S (1997) Comparison of activation of corticospinal neurons and spinal motor neurons by magnetic and electrical transcranial stimulation in the lumbosacral cord of the anaesthetized monkey. Brain 120(Pt 5):839–853PubMedCrossRefGoogle Scholar
  17. Eisen AA, Shtybel W (1990) Clinical experience with transcranial magnetic stimulation. Muscle Nerve 13(11):995–1011PubMedCrossRefGoogle Scholar
  18. Elbert T, Flor H, Birbaumer N, Knecht S, Hampson S, Larbig W, Taub E (1994) Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. Neuroreport 5(18):2593–2597PubMedCrossRefGoogle Scholar
  19. Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81(4):257–262PubMedCrossRefGoogle Scholar
  20. Granit R, Burke RE (1973) The control of movement and posture. Brain Res 53(1):1–28PubMedCrossRefGoogle Scholar
  21. Hall EJ, Flament D, Fraser C, Lemon RN (1990) Non-invasive brain stimulation reveals reorganized cortical outputs in amputees. Neurosci Lett 116(3):379–386PubMedCrossRefGoogle Scholar
  22. Hern JE, Landgren S, Phillips CG, Porter RJ (1962) Selective excitation of corticofugal neurones by surface-anodal stimulation of the baboon’s motor cortex. Physiol 161:73–90Google Scholar
  23. Hess CW, Mills KR, Murray NM (1987) Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol Jul;388:397–419. Erratum in: J Physiol (Lond) 1990 Nov;430:617Google Scholar
  24. Hoffmann KP, Koch KP (2005) Final report on design consideration of tLIFE2. Tech rep, IBMTGoogle Scholar
  25. Jones NF (2002) Concerns about human hand transplantation in the 21st century. J Hand Surg Am 27(5):771–787 (Review)PubMedCrossRefGoogle Scholar
  26. Kaneko K, Kawai S, Fuchigami Y, Shiraishi G, Ito T (1996) Effect of stimulus intensity and voluntary contraction on corticospinal potentials following transcranial magnetic stimulation. J Neurol Sci 139(1):131–136PubMedCrossRefGoogle Scholar
  27. Kernell D (1966) Input resistance, electrical excitability, and size of ventral horn cells in cat spinal cord. Science 152(729):1637–1640PubMedCrossRefGoogle Scholar
  28. Kuiken TA, Li G, Lock BA, Lipschutz RD, Miller LA, Stubblefield KA, Englehart KB (2009) Targeted muscle reinnervation for real-time myoelectric control of multifunction artificial arms. JAMA 301(6):619–628PubMedCrossRefGoogle Scholar
  29. Magistris MR, Rösler KM, Truffert A, Myers JP (1998) Transcranial stimulation excites virtually all motor neurons supplying the target muscle. A demonstration and a method improving the study of motor evoked potentials. Brain 121(Pt 3):437–450PubMedCrossRefGoogle Scholar
  30. Merzenich MM, Jenkins WM (1993) Reorganization of cortical representations of the hand following alterations of skin inputs induced by nerve injury, skin island transfers, and experience. J Hand Ther 6(2):89–104 (Review)PubMedGoogle Scholar
  31. Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1984) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224(4):591–605PubMedCrossRefGoogle Scholar
  32. Micera S, Keller T, Lawrence M, Morari M, Popović DB (2010) Wearable neural prostheses. Restoration of sensory-motor function by transcutaneous electrical stimulation. IEEE Eng Med Biol Mag 29(3):64–69Google Scholar
  33. Mills KR (1991) Magnetic brain stimulation: a tool to explore the action of the motor cortex on single human spinal motoneurones. Trends Neurosci 14(9):401–405 (Review)PubMedCrossRefGoogle Scholar
  34. Navarro X, Krueger TB, Lago N, Micera S, Stieglitz T, Dario P (2005) A critical review of 519 interfaces with the peripheral nervous system for the control of neuroprostheses 520 and hybrid bionic systems. J Peripher Nerv Syst 10:229–258PubMedCrossRefGoogle Scholar
  35. Phillips CG, Porter R (1977) Corticospinal neurones, their role in movement. Monogr Physiol Soc (34):v–xii, 1–450. Review. No abstract availableGoogle Scholar
  36. Rossini PM, Di Stefano E, Stanzione P (1985) Nerve impulse propagation along central and peripheral fast conducting motor and sensory pathways in man. Electroencephalogr Clin Neurophysiol 60(4):320–334PubMedCrossRefGoogle Scholar
  37. Rossini PM, Caramia M, Zarola F (1987) Central motor tract propagation in man: studies with noninvasive, unifocal, scalp stimulation. Brain Res 415(2):211–225PubMedCrossRefGoogle Scholar
  38. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ et al (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92PubMedCrossRefGoogle Scholar
  39. Rossini PM, Caramia MD, Iani C, Desiato MT, Sciarretta G, Bernardi G (1995) Magnetic transcranial stimulation in healthy humans: influence on the behavior of upper limb motor units. Brain Res 676(2):314–324PubMedCrossRefGoogle Scholar
  40. Rossini PM, Micera S, Benvenuto A, Carpaneto J, Cavallo G, Citi L, Cipriani C, Denaro L, Denaro V, Di Pino G, Ferreri F, Guglielmelli E, Hoffmann KP, Raspopovic S, Rigosa J, Rossini L, Tombini M, Dario P (2010) Double nerve intraneural interface implant on a human amputee for robotic hand control. Clin Neurophysiol 121(5):777–783PubMedCrossRefGoogle Scholar
  41. Rothwell JC, Thompson PD, Day BL, Dick JP, Kachi T, Cowan JM, Marsden CD (1987) Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. Brain 110(Pt 5):1173–1190PubMedCrossRefGoogle Scholar
  42. Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76(2):159–200 Review. No abstract availablePubMedGoogle Scholar
  43. Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415PubMedCrossRefGoogle Scholar
  44. Sanes JN, Suner S, Donoghue JP (1990) Dynamic organization of primary motor cortex output to target muscles in adult rats I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp Brain Res 79(3):479–491PubMedCrossRefGoogle Scholar
  45. Spain WJ, Schwindt PC, Crill WE (1991) Post-inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. J Physiol 434:609–626PubMedGoogle Scholar
  46. Théoret H, Halligan E, Kobayashi M, Merabet L, Pascual-Leone A (2004) Unconscious modulation of motor cortex excitability revealed with transcranial magnetic stimulation. Exp Brain Res 155(2):261–264 Epub 2004 Jan 24PubMedCrossRefGoogle Scholar
  47. Wall JT, Kaas JH, Sur M, Nelson RJ, Felleman DJ, Merzenich MM (1986) Functional reorganization in somatosensory cortical areas 3b and 1 of adult monkeys after median nerve repair: possible relationships to sensory recovery in humans. J Neurosci 6:218–233PubMedGoogle Scholar
  48. Wall JT, Xu J, Wang X (2002) Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res Brain Res Rev 39(2–3):181–215PubMedCrossRefGoogle Scholar
  49. Yoshida K, Horch K (1993) Selective stimulation of peripheral nerve fibers using dual intrafascicular electrodes. IEEE Trans Biomed Eng 40:492–494PubMedCrossRefGoogle Scholar
  50. Yoshida K, Horch K (1996) Closed-loop control of ankle position using muscle afferent feedback with functional neuromuscular stimulation. IEEE Trans Biomed Eng 43(2):167–176PubMedCrossRefGoogle Scholar
  51. Ziemann U, Ilić TV, Alle H, Meintzschel F (2004) Cortico-motoneuronal excitation of three hand muscles determined by a novel penta-stimulation technique. Brain 127(Pt 8):1887–1898PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • P. M. Rossini
    • 1
    • 2
  • Jacopo Rigosa
    • 3
  • Silvestro Micera
    • 3
    • 4
  • Giovanni Assenza
    • 1
  • Luca Rossini
    • 2
    • 5
  • Florinda Ferreri
    • 1
    • 6
  1. 1.Department of NeurologyUniversity Campus Bio-MedicoRomeItaly
  2. 2.IRCCS S. Raffaele-PisanaRome and Casa di Cura S. RaffaeleCassinoItaly
  3. 3.Advanced Robotics Technology and Systems LabScuola Superiore Sant’AnnaPisaItaly
  4. 4.Institute for AutomationSwiss Federal Institute of TechnologyZurichSwitzerland
  5. 5.Biomedical Robotics and Biomicrosystems LaboratoryUniversity Campus Bio-MedicoRomeItaly
  6. 6.Department of Clinical NeurophysiologyUniversity of Eastern FinlandKuopioFinland

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