Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods

Limb amputation results in such devastating consequences as loss of motor and sensory functions and phantom limb pain (PLP). Neurostimulation-based approaches have been developed to treat this condition, which provide artificial somatosensory feedback such as peripheral nerve stimulation (PNS), spin...

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Main Authors: Gurgen Soghoyan, Artur R. Biktimirov, Nikita S. Piliugin, Yury Matvienko, Alexander Y. Kaplan, Mikhail Y. Sintsov, Mikhail A. Lebedev
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2024.1466684/full
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author Gurgen Soghoyan
Artur R. Biktimirov
Nikita S. Piliugin
Yury Matvienko
Alexander Y. Kaplan
Alexander Y. Kaplan
Mikhail Y. Sintsov
Mikhail A. Lebedev
Mikhail A. Lebedev
author_facet Gurgen Soghoyan
Artur R. Biktimirov
Nikita S. Piliugin
Yury Matvienko
Alexander Y. Kaplan
Alexander Y. Kaplan
Mikhail Y. Sintsov
Mikhail A. Lebedev
Mikhail A. Lebedev
author_sort Gurgen Soghoyan
collection DOAJ
description Limb amputation results in such devastating consequences as loss of motor and sensory functions and phantom limb pain (PLP). Neurostimulation-based approaches have been developed to treat this condition, which provide artificial somatosensory feedback such as peripheral nerve stimulation (PNS), spinal cord stimulation (SCS), and transcutaneous electrical nerve stimulation (TENS). Yet, the effectiveness of different neurostimulation methods has been rarely tested in the same participants. Meanwhile, such tests would help to select the most effective method or a combination of methods and could contribute to the development of multisensory limb prostheses. In this study, two transhumeral amputees were implanted with stimulating electrodes placed in the medial nerve and over the spinal cord epidurally. PNS and SCS were tested in each participant as approaches to enable tactile and proprioceptive sensations and suppress PLP. Both PNS and SCS induced sensation in different parts of the phantom hand, which correlated with cortical responses detected with electroencephalographic (EEG) recordings. The sensations produced by PNS more often felt natural compared to those produced by SCS. Еvoked response potentials (ERPs) were more lateralized and adapted faster for PNS compared to SCS. In the tasks performed with the bionic hand, neurostimulation-induced sensations enabled discrimination of object size. As the participants practiced with neurostimulation, they improved on the object-size discrimination task and their sensations became more natural. А combination of PNS and TENS enabled sensations that utilized both tactile and proprioceptive information. This combination was effective to convey the perception of object softness. In addition to enabling sensations, neurostimulation led to a decrease in PLP.Clinical trial registrationhttps://clinicaltrials.gov/, identifier, #NCT05650931.
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spelling doaj-art-ec33baf1ea13433cb7da07bb5b6cc1c02025-08-20T01:53:27ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2024-11-011810.3389/fnins.2024.14666841466684Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methodsGurgen Soghoyan0Artur R. Biktimirov1Nikita S. Piliugin2Yury Matvienko3Alexander Y. Kaplan4Alexander Y. Kaplan5Mikhail Y. Sintsov6Mikhail A. Lebedev7Mikhail A. Lebedev8Vladimir Zelman Center for Neurobiology and Brain Rehabilitation, Skolkovo Institute of Science and Technology, Moscow, RussiaLaboratory of Experimental and Translational Medicine, School of Biomedicine, Far Eastern Federal University, Vladivostok, RussiaVladimir Zelman Center for Neurobiology and Brain Rehabilitation, Skolkovo Institute of Science and Technology, Moscow, RussiaMotorica Research Center, Moscow, RussiaVladimir Zelman Center for Neurobiology and Brain Rehabilitation, Skolkovo Institute of Science and Technology, Moscow, RussiaFaculty of Mechanics and Mathematics, Lomonosov Moscow State University, Moscow, RussiaMotorica Research Center, Moscow, RussiaFaculty of Mechanics and Mathematics, Lomonosov Moscow State University, Moscow, RussiaI. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, St. Petersburg, RussiaLimb amputation results in such devastating consequences as loss of motor and sensory functions and phantom limb pain (PLP). Neurostimulation-based approaches have been developed to treat this condition, which provide artificial somatosensory feedback such as peripheral nerve stimulation (PNS), spinal cord stimulation (SCS), and transcutaneous electrical nerve stimulation (TENS). Yet, the effectiveness of different neurostimulation methods has been rarely tested in the same participants. Meanwhile, such tests would help to select the most effective method or a combination of methods and could contribute to the development of multisensory limb prostheses. In this study, two transhumeral amputees were implanted with stimulating electrodes placed in the medial nerve and over the spinal cord epidurally. PNS and SCS were tested in each participant as approaches to enable tactile and proprioceptive sensations and suppress PLP. Both PNS and SCS induced sensation in different parts of the phantom hand, which correlated with cortical responses detected with electroencephalographic (EEG) recordings. The sensations produced by PNS more often felt natural compared to those produced by SCS. Еvoked response potentials (ERPs) were more lateralized and adapted faster for PNS compared to SCS. In the tasks performed with the bionic hand, neurostimulation-induced sensations enabled discrimination of object size. As the participants practiced with neurostimulation, they improved on the object-size discrimination task and their sensations became more natural. А combination of PNS and TENS enabled sensations that utilized both tactile and proprioceptive information. This combination was effective to convey the perception of object softness. In addition to enabling sensations, neurostimulation led to a decrease in PLP.Clinical trial registrationhttps://clinicaltrials.gov/, identifier, #NCT05650931.https://www.frontiersin.org/articles/10.3389/fnins.2024.1466684/fullneuroprostheticsneuromodulationsensory restorationembodimentperipheral nerve stimulationsensory feedback
spellingShingle Gurgen Soghoyan
Artur R. Biktimirov
Nikita S. Piliugin
Yury Matvienko
Alexander Y. Kaplan
Alexander Y. Kaplan
Mikhail Y. Sintsov
Mikhail A. Lebedev
Mikhail A. Lebedev
Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
Frontiers in Neuroscience
neuroprosthetics
neuromodulation
sensory restoration
embodiment
peripheral nerve stimulation
sensory feedback
title Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
title_full Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
title_fullStr Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
title_full_unstemmed Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
title_short Restoration of natural somatic sensations to the amputees: finding the right combination of neurostimulation methods
title_sort restoration of natural somatic sensations to the amputees finding the right combination of neurostimulation methods
topic neuroprosthetics
neuromodulation
sensory restoration
embodiment
peripheral nerve stimulation
sensory feedback
url https://www.frontiersin.org/articles/10.3389/fnins.2024.1466684/full
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