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Electrical Localization of Neural Activity in the Dorsal Horn of the Spinal Cord: A Modeling Study

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Abstract

Intraspinal microstimulation is a means of eliciting coordinated motor responses for restoration of function. However, detailed maps of the neuroanatomy of the human spinal cord are lacking, and it is not clear where electrodes should be implanted. We developed an electrical approach to localize active neurons in the spinal cord using potentials recorded from the surface of the spinal cord. We evaluated this localization method using an analytical model of the spinal cord and two previously developed inverse algorithms (standardized low resolution brain electromagnetic tomography (sLORETA) and a locally optimal source (LOS) method). The results support electrical source localization as a feasible imaging approach for localizing (within 300 μm) active neurons in the spinal cord. The LOS method could localize the source when 16 recording electrodes were placed on the dorsolateral aspect of the cord and the noise level was 2%. When recording electrodes were positioned around the entire circumference of the spinal cord, either localization method could localize the source, even at 15% noise. Finally, localization error was not sensitive to inaccuracies in the expected electrode positions or the electrical parameters of the forward model, but was sensitive to a geometrical modification of the forward model in one case.

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References

  1. Altman, K. W., and R. Plonsey. Development of a model for point source electrical fibre bundle stimulation. Med. Biol. Eng. Comput. 26:466–475, 1988.

    Google Scholar 

  2. Andersson, O., and S. Grillner. Peripheral control of the cat’s step cycle. I. Phase dependent effects of ramp-movements of the hip during “fictive locomotion.” Acta. Physiol. Scand. 113:89–101, 1981.

    Article  Google Scholar 

  3. Barbeau, H., D. A. McCrea, M. J. O’Donovan, S. Rossignol., W. M. Grill, and M. A. Lemay. Tapping into spinal circuits to restore motor function. Brain Res. Brain Res. Rev. 30:27–51, 1999.

    Google Scholar 

  4. Beall, J. E., A. E. Applebaum, R. D. Foreman, and W. D. Willis. Spinal cord potentials evoked by cutaneous afferents in the monkey. J. Neurophysiol. 40:199–211, 1977.

    Google Scholar 

  5. Brindley, G. S. History of the sacral anterior root stimulator, 1969–1982. Neurourol. Urodyn. 12:481–483, 1993.

    Google Scholar 

  6. Cuffin, B. N. A comparison of moving dipole inverse solutions using EEG’s and MEG’s. IEEE Trans. Biomed. Eng. 32:905–910, 1985.

    Google Scholar 

  7. DiMarco, A. F., R. P. Onders, K. E. Kowalski, M. E. Miller, S. Ferek., and J. T. Mortimer. Phrenic nerve pacing in a tetraplegic patient via intramuscular diaphragm electrodes. Am. J. Respir. Crit. Care Med. 166:1604–1606, 2002.

    Google Scholar 

  8. Giszter, S. F., E. Loeb., F. A. Mussa-Ivaldi, and E. Bizzi. Repeatable spatial maps of a few force and joint torque patterns elicited by microstimulation applied throughout the lumbar spinal cord of the spinal frog. Hum. Mov. Sci. 19:597–626, 2000.

    Google Scholar 

  9. Giszter, S. F., W. M. Grill, M. A. Lemay, V. K. Mushahwar, and A. Prochazka. Intraspinal microstimulation: Techniques, perspectives, and prospects for FES. In: Neural Prostheses for Restoration of Sensory and Motor Function, Methods and New Frontiers in Neuroscience Series, edited by J. K. Chapin and K. A. Moxon. Boca Raton: CRC Press, 2001, pp. 101– 138.

  10. Glenn, W. W., and M. L. Phelps. Diaphragm pacing by electrical stimulation of the phrenic nerve. Neurosurgery 17:974–984, 1985.

    Google Scholar 

  11. Gorodnitsky, I. F., J. S. George, and B. D. Rao. Neuromagnetic source imaging with FOCUSS: A recursive weighted minimum norm algorithm. Electroencephalogr. Clin. Neurophysiol. 95:231–251, 1995.

    Google Scholar 

  12. Grill, W. M., and B. Wang., Mapping knee torques evoked by intraspinal microstimulation. Proceedings of the 19th Annual International Conference of IEEE-EMBS:1950–1951, 1997.

  13. Grill, W. M., K. J. Gustafson, and M. A. Moffitt. Mapping spinal neurons active during hindlimb flexion withdrawal reflex in cat using c-Fos expression. Program No. 667.10. 2002 Abstract Viewer/Itinerary Planner. Washington., DC: Society for Neuroscience, 2002; CD-ROM, 2002.

  14. Grillner, S. On the generation of locomotion in the spinal dogfish. Exp. Brain Res. 20:459–470, 1974.

    Google Scholar 

  15. Gustafson, K. J., G. H. Creasey, and W. M. Grill. A catheter based method to activate urethral sensory nerve fibers. J. Urol. 170:126–129, 2003.

    Google Scholar 

  16. Hämäläinen, M. S., and R. J. Ilmoniemi. Interpreting measured magnetic fields of the brain: Estimates of current distributions, Technical Report TKK-F-A559, Finland: Helsinki University of Technology, 1984.

  17. Hansen, P. C. Analysis of discrete Ill-Posed problems by means of the L-Curve. SIAM Rev. 34:561–580, 1992.

    MATH  MathSciNet  Google Scholar 

  18. He, B., D. Yao., J. Lian., and D. Wu. An equivalent current source model and laplacian weighted minimum norm current estimates of brain electrical activity. IEEE Trans. Biomed. Eng. 49:277–288, 2002.

    Google Scholar 

  19. Hori, J., and B. He. Equivalent dipole source imaging of brain electric activity by means of parametric projection filter. Ann. Biomed. Eng. 29:436–445, 2001.

    Google Scholar 

  20. Huang, M., C. J. Aine, S. Supek., E. Best., D. Ranken., and E. R. Flynn. Multi-start downhill simplex method for spatio-temporal source localization in magnetoencephalography. Electroencephalogr. Clin. Neurophysiol. 108:32–44, 1998.

    Google Scholar 

  21. Jeffs, B., R. Leahy., and M. Singh. An evaluation of methods for neuromagnetic image reconstruction. IEEE Trans. Biomed. Eng. 34:713–723, 1987.

    Google Scholar 

  22. Kameyama, T., Y. Hashizume., and G. Sobue. Morphologic features of the normal human cadaveric spinal cord. Spine 21:1285–1290, 1996.

    Google Scholar 

  23. Laarne, P., J. Hyttinen., S. Dodel., J. Malmivuo., and H. Eskola. Accuracy of two dipolar inverse algorithms applying reciprocity for forward calculation. Comput. Biomed. Res. 33:172–185, 2000.

    Google Scholar 

  24. Lemay, M. A., and W. M. Grill. Modularity of motor output evoked by intraspinal microstimulation in cats. J. Neurophysiol. 91:502–514, 2004.

    Google Scholar 

  25. Lemay, M. A., J. E. Galagan, N. Hogan., and E. Bizzi. Modulation and vectorial summation of the spinalized frog’s hindlimb end-point force produced by intraspinal electrical stimulation of the cord. IEEE Trans. Neural. Systems Rehabil. Eng. 9:12–23, 2001.

    Google Scholar 

  26. Levinsson, A., H. Holmberg., J. Broman., M. Zhang., and J. Schouenborg. Spinal sensorimotor transformation: Relation between cutaneous somatotopy and a reflex network. J. Neurosci. 22:8170–8182, 2002.

    Google Scholar 

  27. Lozano, A. M., J. Dostrovsky., R. Chen., and P. Ashby. Deep brain stimulation for Parkinson’s disease: Disrupting the disruption. Lancet Neurol. 1:225–231, 2002.

    Google Scholar 

  28. Malisza, K. L., and P. W. Stroman. Functional imaging of the rat cervical spinal cord. J. Magn. Reson. Imaging. 16:553–558, 2002.

    Google Scholar 

  29. Meier, J. H., W. L. Rutten, and H. B. Boom. Extracellular potentials from active myelinated fibers inside insulated and noninsulated peripheral nerve. IEEE Trans. Biomed. Eng. 45:1146–1153, 1998.

    Google Scholar 

  30. Mitzdorf, U. Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65:37–100, 1985.

    Google Scholar 

  31. Mushahwar, V. K., D. M. Gillard, M. J. Gauthier, and A. Prochazka. Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements. IEEE Trans. Neural Systems Rehabil. Eng. 10:68–81, 2002.

    Google Scholar 

  32. Nicholson, P. W. Experimental models for current conduction in an anisotropic medium. IEEE Trans. Biomed. Eng. 14:55–56, 1967.

    Google Scholar 

  33. Noga, B. R., P. A. Fortier, D. J. Kriellaars, X. Dai., G. R. Detillieux, and L. M. Jordan. Field potential mapping of neurons in the lumbar spinal cord activated following stimulation of the mesencephalic locomotor region. J. Neurosci. 15:2203–2217, 1995.

    Google Scholar 

  34. Pascual-Marqui, R. D. Reply to comments made by R. Grave De Peralta Menendez and S. I. Gozalez Andino. Int. J. Bioelectromagnetism 1:at http://www.ee.tut.fi/rgi/ijbem/volume1/ number2/html/pascual.htm, 1999.

  35. Pascual-Marqui, R. D. Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find. Exp. Clin. Pharmacol. 24(SupplD):5–12, 2002.

    Google Scholar 

  36. Pascual-Marqui, R. D., C. M. Michel, and D. Lehmann. Low resolution electromagnetic tomography: A new method for localizing electrical activity in the brain. Int. J. Psychophysiol. 18:49–65, 1994.

    Google Scholar 

  37. Peckham, P. H., K. L. Kilgore, M. W. Keith, A. M. Bryden, N. Bhadra., and F. W. Montague. An advanced neuroprosthesis for restoration of hand and upper arm control using an implantable controller. J. Hand. Surg. [Am]. 27:265–276, 2002.

    Google Scholar 

  38. Phillips, J. W., R. M. Leahy, and J. C. Mosher. MEG-based imaging of focal neuronal current sources. IEEE Trans. Med. Imaging. 16:338–348, 1997.

    Google Scholar 

  39. Porszasz, R., N. Beckmann., K. Bruttel., L. Urban., and M. Rudin. Signal changes in the spinal cord of the rat after injection of formalin into the hindpaw: Characterization using functional magnetic resonance imaging. Proc. Natl Acad. Sci. USA 94:5034–5039, 1997.

    Google Scholar 

  40. Ranck Jr., J. B., and S. L. BeMent. The specific impedance of the dorsal columns of cat: An anisotropic medium. Exp. Neurol. 11:451–463, 1965.

    Google Scholar 

  41. Schouenborg, J. Functional and topographical properties of field potentials evoked in rat dorsal horn by cutaneous C-fibre stimulation. J. Physiol. 356:169–192, 1984.

    Google Scholar 

  42. Sherrington, C. S. Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J. Physiol. 40:28–121, 1910.

    Google Scholar 

  43. Stroman, P. W., B. Tomanek., V. Krause., U. N. Frankenstein, and K. L. Malisza. Mapping of neuronal function in the healthy and injured human spinal cord with spinal fMRI. Neuroimage 17:1854–1860, 2002.

    Google Scholar 

  44. Supek, S., and C. J. Aine. Simulation studies of multiple dipole neuromagnetic source localization: Model order and limits of source resolution. IEEE Trans. Biomed. Eng. 40:529–540, 1993.

    Google Scholar 

  45. Tikhonov, A. N., and V. Y. Arsenin. Solutions of Ill-Posed Problems, New York: Wiley, 1977.

    MATH  Google Scholar 

  46. Tresch, M. C., and E. Bizzi. Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation. Exp. Brain Res. 129:401–416, 1999.

    Google Scholar 

  47. Vanderhorst, V. G., and G. Holstege. Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat. J. Comp. Neurol. 382:46–76, 1997.

    Google Scholar 

  48. Willis, W. D., and R. E. Coggeshall. Sensory Mechanisms of the Spinal Cord, 2nd ed. New York: Plenum, 1991.

    Google Scholar 

  49. Willis, W. D., M. A. Weir, R. D. Skinner, and R. N. Bryan. Differential distribution of spinal cord field potentials. Exp. Brain Res. 17:169–176, 1973.

    Google Scholar 

  50. Wilson, O. B., J. W. Clark Jr., N. Ganapathy., and T. L. Harman. Potential field from an active nerve in an inhomogeneous, anisotropic volume conductor–the forward problem. IEEE Trans. Biomed. Eng. 32:1033–1041, 1985.

    Google Scholar 

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Correspondence to Warren M. Grill.

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Moffitt, M.A., Grill, W.M. Electrical Localization of Neural Activity in the Dorsal Horn of the Spinal Cord: A Modeling Study. Ann Biomed Eng 32, 1694–1709 (2004). https://doi.org/10.1007/s10439-004-7822-5

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