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Restoration of sensory feedback from the foot and reduction of phantom limb pain via closed-loop spinal cord stimulation

Nature Biomedical Engineering (2023)Cite this article

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A Publisher Correction to this article was published on 28 December 2023

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Abstract

Restoring somatosensory feedback in individuals with lower-limb amputations would reduce the risk of falls and alleviate phantom limb pain. Here we show, in three individuals with transtibial amputation (one traumatic and two owing to diabetic peripheral neuropathy), that sensations from the missing foot, with control over their location and intensity, can be evoked via lateral lumbosacral spinal cord stimulation with commercially available electrodes and by modulating the intensity of stimulation in real time on the basis of signals from a wireless pressure-sensitive shoe insole. The restored somatosensation via closed-loop stimulation improved balance control (with a 19-point improvement in the composite score of the Sensory Organization Test in one individual) and gait stability (with a 5-point improvement in the Functional Gait Assessment in one individual). And over the implantation period of the stimulation leads, the three individuals experienced a clinically meaningful decrease in phantom limb pain (with an average reduction of nearly 70% on a visual analogue scale). Our findings support the further clinical assessment of lower-limb neuroprostheses providing somatosensory feedback.

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Fig. 1: Schematic of the closed-loop SCS system used in this study.
Fig. 2: SCS evokes percepts in the missing limb.
Fig. 3: Psychophysical assessment of evoked sensations.
Fig. 4: Closed-loop sensory feedback improves postural stability.
Fig. 5: Closed-loop sensory feedback improves gait stability.
Fig. 6: SCS reduces PLP.

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Data availability

Source data for the figures in this study are available in the Data Archive for the Brain Initiative, with the identifier https://doi.org/10.18120/8qby-hk82 (ref. 59). The raw and analysed datasets generated during the study are available for research purposes from the corresponding author on reasonable request.

Code availability

The custom code used to generate figures for this manuscript is available at https://github.com/pitt-rnel/NatureBME2023_SCSLowerLimb.

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Acknowledgements

We dedicate this work to our dear friend and colleague Sliman J. Bensmaia, without whose support, insight and passion for science and mentorship this project would not have been possible. We wish to thank P. Sparto for his assistance with the blinded review of functional outcome measures. All authors acknowledge support for the research described in this study from the National Institutes of Health cooperative agreement UH3NS100541. B.A.P. acknowledges support for the research described in this study from National Institutes of Health training grant F30HD098794. B.B. acknowledges support for the research described in this study from Swiss National Science Foundation Doc.Mobility fellowship P1FRP3_188027.

Author information

Author notes

  1. These authors contributed equally: Ameya C. Nanivadekar, Rohit Bose, Bailey A. Petersen.

  2. Deceased: Sliman J. Bensmaia.

Authors and Affiliations

  1. Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA

    Ameya C. Nanivadekar, Rohit Bose, Bailey A. Petersen, Devapratim Sarma, Tyler J. Madonna, Beatrice Barra, Juhi Farooqui, Ashley N. Dalrymple, Michael L. Boninger, Marco Capogrosso, Douglas J. Weber & Lee E. Fisher

  2. Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA

    Ameya C. Nanivadekar, Rohit Bose, Bailey A. Petersen, Michael L. Boninger, Marco Capogrosso & Lee E. Fisher

  3. Center for the Neural Basis of Cognition, Pittsburgh, PA, USA

    Ameya C. Nanivadekar, Rohit Bose, Bailey A. Petersen, Juhi Farooqui, Michael L. Boninger, Marco Capogrosso & Lee E. Fisher

  4. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA

    Elizaveta V. Okorokova & Sliman J. Bensmaia

  5. Department of Mechanical Engineering, Carnegie Mellon University, Pittsburgh, PA, USA

    Devapratim Sarma, Ashley N. Dalrymple & Douglas J. Weber

  6. Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA

    Tyler J. Madonna, Isaiah Levy, Eric R. Helm, Michael L. Boninger & Lee E. Fisher

  7. Department of Neuroscience and Movement Science, University of Fribourg, Fribourg, Switzerland

    Beatrice Barra

  8. Department of Biomedical Engineering, University of Utah, Salt Lake City, UT, USA

    Ashley N. Dalrymple

  9. Department of Physical Medicine and Rehabilitation, University of Utah, Salt Lake City, UT, USA

    Ashley N. Dalrymple

  10. Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA, USA

    Vincent J. Miele & Marco Capogrosso

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Contributions

L.E.F., D.J.W., S.J.B. and M.L.B. conceived the study and designed the research. A.C.N., R.B., B.A.P., D.S., T.J.M., B.B., J.F., A.N.D., I.L. and L.E.F. performed experiments. E.R.H. and V.J.M. performed implantation procedures. E.R.H., V.J.M., M.L.B. and I.L. managed medical care and oversight for the study. A.C.N., R.B., B.A.P. and E.V.O. performed data analysis. L.E.F., A.C.N., R.B., B.A.P., E.V.O., S.J.B. and M.C. wrote the manuscript with input from all authors. L.E.F. supervised the study.

Corresponding author

Correspondence to Lee E. Fisher.

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Nature Biomedical Engineering thanks Rickard Brånemark, Troels S. Jensen, Winfried Mayr, Solomon Tesfaye and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Sensory integrity and impairments for each participant.

Shaded regions indicate areas with either impaired (light) or absent (dark) light touch sensation as determined by clinical neurological testing.

Extended Data Fig. 2 Heatmaps showing the rate of occurrence of sensations in the missing limb across weeks.

Darker shades indicate higher rate of occurrence of sensations in that location. No testing was done on week 11 for Participant 3.

Extended Data Fig. 3 Comparison of the threshold amplitude that evoked sensation in the missing limb (with co-activation in the residual limb) and the threshold amplitude that evoked sensation only in the residual limb.

The threshold amplitude for each testing day was determined by increasing the stimulation amplitude in 0.5 or 1 mA steps and asking the participants to report the location where they perceived the evoked sensation. Error bars show the mean ± standard deviation across multiple days (N = 4 for Participant 1, N = 13 for Participant 2 and N = 8 for Participant 3).

Extended Data Fig. 4 Dermatomal activation by electrodes located at different vertebrae levels for Participant 2 and Participant 3.

The left image shows the expected dermatomal innervation in the leg22. In the right, the horizontal bars indicate different dermatomes and the white ovals indicate the approximate electrode position that evoked sensations in that dermatome with respect to the vertebrae level. Participant 1 had substantial lead migration across weeks, making it challenging to precisely define the location of the electrodes with respect to vertebrae levels, so we have not included those results.

Extended Data Fig. 5 Percept quality of evoked sensations in the missing limb.

The participants were given a list of 13 natural descriptors and 5 paresthetic descriptors to describe the quality of the sensation. The top panel shows the frequency of each descriptor for the two evoked sensations for each participant shown in Fig. 2a. For all reported sensations, we stimulated via each electrode with a 1-sec long pulse train. The bottom panel shows the total number of descriptors used to describe the sensations each week.

Extended Data Fig. 6 Additional results from psychophysical discrimination assessment.

a, Variation of Weber fraction for different electrodes in Participant 1 and 2 as a function of the reference amplitude in the discrimination task. b, Variation of JND for the same electrodes in Participants 1 and 2 as a function of the reference amplitude. Participant 3 was discarded from these analyses due to insufficient data points.

Extended Data Fig. 7 Full results of Sensory Organization Test (SOT).

a, Participant 2 performed the SOT without stimulation (light blue) with sham stimulation (that is, stimulation in the residual limb only, gray) and with stimulation (stimulation in the prosthetic foot, dark blue). Sham stimulation substantially decreased performance for three of six conditions (with greater than minimum detectable change [MDC, 3.98]), suggesting that stimulation on the residual limb alone was not sufficient to improve performance. b, Participant 3 performed the SOT without stimulation (light magenta) and with stimulation (dark magenta). Both Participant 2 and Participant 3 exhibited improved performance on conditions with platform sway and eyes closed (+5.12 Participant 2, +9.60 Participant 3) and with visual surround sway (+4.04 Participant 2, +13.39 Participant 3). Both participants, however, exhibited decreased performance with stimulation during static standing with eyes closed (−6.25 Participant 2, −4.32 Participant 3). Additionally, Participant 3 had worse performance on static standing with eyes open with stimulation (−4.13). Change in median values reported. * represents a MDC, ** represents a clinically meaningful difference (>8.0).

Extended Data Fig. 8 McGill Pain Questionnaire results.

a, Weekly McGill Pain Questionnaire results. b, McGill Pain Questionnaire score before the implant and 1-month post-explant. The pre-implant score for Participant 2 was not recorded and we did not perform testing on week 11 for Participant 3 (indicated by the dashed line).

Supplementary information

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Video

Video of participant 3 walking with real-time somatosensory feedback delivered via SCS.

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Nanivadekar, A.C., Bose, R., Petersen, B.A. et al. Restoration of sensory feedback from the foot and reduction of phantom limb pain via closed-loop spinal cord stimulation. Nat. Biomed. Eng (2023). https://doi.org/10.1038/s41551-023-01153-8

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