Phantom sensations generated by thalamic microstimulation

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Abstract

Many amputees have a sense of their missing ‘phantom’ limb1,2,3. Amputation can alter the representation of the body's surface in the cerebral cortex4,5,6,7,8,9,10,11,12,13,14 and thalamus15,16, but it is unclear how these changes relate to such phantom sensations. One possibility is that, in amputees who experience phantom sensations, the region of the thalamus that originally represented the missing limb remains functional and can give rise to phantom sensations even when some thalamic ‘limb’ neurons begin to respond to stimulation of other body regions. Here we use microelectrode recording and microstimulation during functional stereotactic mapping of the ventrocaudal thalamus in amputees to determine both the responses of the neurons to stimulation of the skin and the perceptual effects of electrical activation of these neurons. Thalamic mapping revealed an unusually large thalamic stump representation, consistent with the findings from animal experiments. We also found that thalamic stimulation in amputees with a phantom limb could evoke phantom sensations, including pain, even in regions containing neurons responsive to tactile stimulation of the stump. These findings support the hypothesis that the thalamic representation of the amputated limb remains functional in amputees with phantoms.

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Figure 1: Results from patient 4 who had both stump and phantom pain after an amputation above the knee.
Figure 2: A portion of one electrode trajectory in each of two patients with phantom pain.

References

  1. 1

    Sherman, R. A., Sherman, C. J. & Parker, L. Chronic phantom and stump pain among American veterans: results of a survey. Pain 18, 83–95 (1984).

  2. 2

    Carlen, P. L., Wall, P. D., Nadvorna, H. & Steinbach, T. Phantom limbs and related phenomena in recent traumatic amputations. Neuroloby 28, 211–217 (1978).

  3. 3

    Melzack, R. Phantom limbs and the concept of a neuromatrix. Trends Neurosci. 13, 88–92 (1990).

  4. 4

    Calford, M. B. & Tweedale, R. Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. Somatosens. Mot. Res. 8, 249–260 (1991).

  5. 5

    Wall, J. T., Huerta, M. F. & Kaas, J. H. Changes in the cortical map of the hand following postnatal median nerve injury in monkeys: Modification of somatotopic aggregates. J. Neurosci. 12, 3445–3455 (1992).

  6. 6

    Rasmusson, D. D. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J. Comp. Neurol. 205, 313–326 (1982).

  7. 7

    Flor, H.et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482–484 (1995).

  8. 8

    Elbert, T.et al. Extensive reorganization of the somatosensory cortex in adult humans after nervous system injury. Neuroreport 5, 2593–2597 (1994).

  9. 9

    Yang, T. T.et al. Noninvasive detection of cerebral plasticity in adult human somatosensory cortex. Neuroreport 5, 701–704 (1994).

  10. 10

    Kew, J. J. M.et al. Abnormal access of axial vibrotactile input to deafferented somatosensory cortex in human upper limb amputees. J. Neurophysiol. 77, 2753–2764 (1997).

  11. 11

    Merzenich, M. M.et al. Topographic reorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 33–55 (1983).

  12. 12

    Pons, T. P.et al. Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252, 1857–1860 (1991).

  13. 13

    Florence, S. L. & Kaas, J. H. Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J. Neurosci. 15, 8083–8095 (1995).

  14. 14

    Merzenich, M. M.et al. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224, 591–605 (1984).

  15. 15

    Rasmusson, D. Changes in the organization of the ventroposterior lateral thalamic nucleus after digit removal in adult raccoon. J. Comp. Neurol. 364, 92–103 (1996).

  16. 16

    Wall, P. D. & Egger, M. D. Formation of new connexions in adult rat brains after partial deafferentation. Nature 232, 542–545 (1971).

  17. 17

    Tasker, R. R. & Kiss, Z. H. T. The role of the thalamus in functional neurosurgery. Neurosurg. Clin. N. Am. 6, 73–104 (1995).

  18. 18

    Tsoukatos, J., Davis, K. D., Tasker, R. R., Lozano, A. M. & Dostrovsky, J. O. Deafferentation and local damage give rise to bursting activity in thalamus of awake patients. Soc. Neurosci. Abstr. 22, 98 (1996).

  19. 19

    Lenz, F. A.et al. Single-unit analysis of the human ventral thalamic nuclear group: Somatosensory responses. J. Neurophysiol. 59, 299–316 (1988).

  20. 20

    Davis, K. D., Kiss, Z. H. T., Tasker, R. R. & Dostrovsky, J. O. Thalamic stimulation-evoked sensations in chronic pain patients and in nonpain (movement disorder) patients. J. Neurophysiol. 75, 1026–1037 (1996).

  21. 21

    Lenz, F. A.et al. Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. J. Neurophysiol. 72, 1570–1587 (1994).

  22. 22

    Kiss, Z. H. T., Dostrovsky, J. O. & Tasker, R. R. Plasticity in human somatosensory thalamus as a result of deafferentation. Stereotact. Funct. Neurosurg. 62, 153–163 (1994).

  23. 23

    Halligan, P. W., Marshall, J. C., Wade, D. T., Davey, J. & Morrison, D. Thumb in cheek? Sensory reorganization and perceptual plasticity after limb amputation. Neuroreport 4, 233–236 (1993).

  24. 24

    Aglioti, S., Cortese, F. & Franchini, C. Rapid sensory remapping in the adult human brain as inferred from phantom breast perception. Neuroreport 5, 473–476 (1994).

  25. 25

    Knecht, S.et al. Cortical reorganization in human amputees and mislocalization of painful stimuli to the phantom limb. Neurosci. Lett. 201, 262–264 (1995).

  26. 26

    Clarke, S., Regli, L., Janzer, R. C., Assal, G. & De Tribolet, N. Phantom face: Conscious correlate of neural reorganization after removal of primary sensory neurones. Neuroreport 7, 2853–2857 (1996).

  27. 27

    Doetsch, G. S. Progressive changes in cutaneous trigger zones for sensation referred to a phantom hand: a case report and review with implications for cortical reorganization. Somatosens. Mot. Res. 14, 6–16 (1997).

  28. 28

    Ramachandran, V. S. Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. Proc. Natl Acad. Sci. USA 90, 10413–10420 (1993).

  29. 29

    Lenz, F. A.et al. Methods for microstimulation and recording of single neurons and evoked potentials in the human central nervous system. J. Neurosurg. 68, 630–634 (1988).

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Acknowledgements

We thank F. Lenz for assistance with data collection from two of the patients; M.Teofilo for technical assistance with computer reconstructions of patient data; and A. D. Craig and J.Katz for comments on an earlier draft of this manuscript. This work was supported by the Medical Research Council of Canada and NIH.

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Correspondence to Karen D. Davis.

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