Literature DB >> 32759488

A comprehensive model-based framework for optimal design of biomimetic patterns of electrical stimulation for prosthetic sensation.

Karthik Kumaravelu1, Tucker Tomlinson2, Thierri Callier3, Joseph Sombeck4, Sliman J Bensmaia3, Lee E Miller2,4,5, Warren M Grill1,6,7,8.   

Abstract

OBJECTIVE: Touch and proprioception are essential to motor function as shown by the movement deficits that result from the loss of these senses, e.g. due to neuropathy of sensory nerves. To achieve a high-performance brain-controlled prosthetic arm/hand thus requires the restoration of somatosensation, perhaps through intracortical microstimulation (ICMS) of somatosensory cortex (S1). The challenge is to generate patterns of neuronal activation that evoke interpretable percepts. We present a framework to design optimal spatiotemporal patterns of ICMS (STIM) that evoke naturalistic patterns of neuronal activity and demonstrate performance superior to four previous approaches. APPROACH: We recorded multiunit activity from S1 during a center-out reach task (from proprioceptive neurons in Brodmann's area 2) and during application of skin indentations (from cutaneous neurons in Brodmann's area 1). We implemented a computational model of a cortical hypercolumn and used a genetic algorithm to design STIM that evoked patterns of model neuron activity that mimicked their experimentally-measured counterparts. Finally, from the ICMS patterns, the evoked neuronal activity, and the stimulus parameters that gave rise to it, we trained a recurrent neural network (RNN) to learn the mapping function between the physical stimulus and the biomimetic stimulation pattern, i.e. the sensory encoder to be integrated into a neuroprosthetic device. MAIN
RESULTS: We identified ICMS patterns that evoked simulated responses that closely approximated the measured responses for neurons within 50 µm of the electrode tip. The RNN-based sensory encoder generalized well to untrained limb movements or skin indentations. STIM designed using the model-based optimization approach outperformed STIM designed using existing linear and nonlinear mappings. SIGNIFICANCE: The proposed framework produces an encoder that converts limb state or patterns of pressure exerted onto the prosthetic hand into STIM that evoke naturalistic patterns of neuronal activation.

Entities:  

Mesh:

Year:  2020        PMID: 32759488      PMCID: PMC8559728          DOI: 10.1088/1741-2552/abacd8

Source DB:  PubMed          Journal:  J Neural Eng        ISSN: 1741-2552            Impact factor:   5.379


  82 in total

1.  Selective microstimulation of central nervous system neurons.

Authors:  C C McIntyre; W M Grill
Journal:  Ann Biomed Eng       Date:  2000-03       Impact factor: 3.934

Review 2.  NEURON: a tool for neuroscientists.

Authors:  M L Hines; N T Carnevale
Journal:  Neuroscientist       Date:  2001-04       Impact factor: 7.519

Review 3.  Large-scale recording of neuronal ensembles.

Authors:  György Buzsáki
Journal:  Nat Neurosci       Date:  2004-05       Impact factor: 24.884

4.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements.

Authors:  M J Prud'homme; J F Kalaska
Journal:  J Neurophysiol       Date:  1994-11       Impact factor: 2.714

5.  Thalamic input to areas 3a and 2 in monkeys.

Authors:  D P Friedman; E G Jones
Journal:  J Neurophysiol       Date:  1981-01       Impact factor: 2.714

6.  A neural network that finds a naturalistic solution for the production of muscle activity.

Authors:  David Sussillo; Mark M Churchland; Matthew T Kaufman; Krishna V Shenoy
Journal:  Nat Neurosci       Date:  2015-06-15       Impact factor: 24.884

Review 7.  Challenges and opportunities for next-generation intracortically based neural prostheses.

Authors:  Vikash Gilja; Cindy A Chestek; Ilka Diester; Jaimie M Henderson; Karl Deisseroth; Krishna V Shenoy
Journal:  IEEE Trans Biomed Eng       Date:  2011-01-20       Impact factor: 4.538

8.  High-performance neuroprosthetic control by an individual with tetraplegia.

Authors:  Jennifer L Collinger; Brian Wodlinger; John E Downey; Wei Wang; Elizabeth C Tyler-Kabara; Douglas J Weber; Angus J C McMorland; Meel Velliste; Michael L Boninger; Andrew B Schwartz
Journal:  Lancet       Date:  2012-12-17       Impact factor: 79.321

9.  Multi-electrode stimulation in somatosensory cortex increases probability of detection.

Authors:  Boubker Zaaimi; Ricardo Ruiz-Torres; Sara A Solla; Lee E Miller
Journal:  J Neural Eng       Date:  2013-08-28       Impact factor: 5.379

Review 10.  Biological and bionic hands: natural neural coding and artificial perception.

Authors:  Sliman J Bensmaia
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-19       Impact factor: 6.237

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  4 in total

1.  Stoney vs. Histed: Quantifying the spatial effects of intracortical microstimulation.

Authors:  Karthik Kumaravelu; Joseph Sombeck; Lee E Miller; Sliman J Bensmaia; Warren M Grill
Journal:  Brain Stimul       Date:  2021-11-30       Impact factor: 8.955

Review 2.  The science and engineering behind sensitized brain-controlled bionic hands.

Authors:  Chethan Pandarinath; Sliman J Bensmaia
Journal:  Physiol Rev       Date:  2021-09-20       Impact factor: 37.312

3.  Normalization by valence and motivational intensity in the sensorimotor cortices (PMd, M1, and S1).

Authors:  Zhao Yao; John P Hessburg; Joseph Thachil Francis
Journal:  Sci Rep       Date:  2021-12-20       Impact factor: 4.379

4.  A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys.

Authors:  Kantapon Pum Wiboonsaksakul; Dale C Roberts; Charles C Della Santina; Kathleen E Cullen
Journal:  PLoS Biol       Date:  2022-09-14       Impact factor: 9.593

  4 in total

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