Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans

  1. Calogero Maria Oddo  Is a corresponding author
  2. Stanisa Raspopovic
  3. Fiorenzo Artoni
  4. Alberto Mazzoni
  5. Giacomo Spigler
  6. Francesco Petrini
  7. Federica Giambattistelli
  8. Fabrizio Vecchio
  9. Francesca Miraglia
  10. Loredana Zollo
  11. Giovanni Di Pino
  12. Domenico Camboni
  13. Maria Chiara Carrozza
  14. Eugenio Guglielmelli
  15. Paolo Maria Rossini
  16. Ugo Faraguna
  17. Silvestro Micera  Is a corresponding author
  1. Scuola Superiore Sant'Anna, Italy
  2. École Polytechnique Fédérale de Lausanne, Switzerland
  3. Università Campus Bio-Medico di Roma, Italy
  4. IRCCS San Raffaele Pisana, Italy
  5. Catholic University of The Sacred Heart, Italy
  6. Azienda Ospedaliero-Universitaria Pisana, Italy
  7. IRCCS Stella Maris Foundation, Italy
  8. Università di Pisa, Italy
12 figures and 1 video

Figures

Experimental setup and performance metrics.

(a) Sensorized artificial finger and tactile stimulation platform. (b) Tactile stimuli that were used in the three-alternative forced-choice (3AFC) psychophysical protocol and the raster plot of …

https://doi.org/10.7554/eLife.09148.003
Mechano-neuro-transduction process.

(a) MEMS sensor with 4 transducing piezoresistors implanted at the base of a cross-shaped structure (sensor piezoresistive outputs Sx+ and Sx- are represented in blue and in green, respectively), …

https://doi.org/10.7554/eLife.09148.004
Responses of intact subjects during the 3AFC psychophysical protocol with percutaneous electrical microstimulation of the median nerve.

Each column reports results of the analyses on individual subject basis. (a) Each panel displays the confusion matrix of behavioral responses relative to the four intact subjects with …

https://doi.org/10.7554/eLife.09148.005
Figure 4 with 5 supplements
Cortical response to mechanical and electrical stimulation using a surface with 1.5 mm SP.

(a) Grand average event related potentials (ERPs) of all subjects (n = 4) for both substitutive neuromorphic electrical (red) and natural mechanical tactile (blue) stimulation, ranging from -1500 to …

https://doi.org/10.7554/eLife.09148.007
Figure 4—figure supplement 1
Grand average event related potentials (ERPs) of all subjects (n = 4) at the FC1 electrode for both the substitutive neuromorphic electrical (red) and natural mechanical tactile (black) stimulation, in the -150 to 350 ms window with respect to stimulus onset, with confidence interval bars.

The horizontal black bar indicates the time window (210–240 ms) when the evoked potential reached significance compared with the prestimulus voltage (2 Standard Deviations from the mean prestimulus …

https://doi.org/10.7554/eLife.09148.008
Figure 4—figure supplement 2
Sample size computation based on the effect size of the prestimulus and the evoked activity within the significant time-window for the electrical microstimulation.
https://doi.org/10.7554/eLife.09148.009
Figure 4—figure supplement 3
Sample size computation based on the effect size of the prestimulus and the evoked activity within the significant time-window for the mechanical stimulation.
https://doi.org/10.7554/eLife.09148.010
Figure 4—figure supplement 4
Sample size computation based on the prestimulus effect sizes preceding the electrical microstimulation and the mechanical stimulation.
https://doi.org/10.7554/eLife.09148.011
Figure 4—figure supplement 5
Sample size computation based on the effect size of the stimulus voltages (ERPs within the significant time-window after the electrical microstimulation, and after the mechanical stimulation).
https://doi.org/10.7554/eLife.09148.012
Cortical localization of a 1 Hz electrical microstimulation sensory evoked potential.

(a) Butterfly plot of SEPs for all 64 channels of one subject (M4). All traces are aligned to the electrical stimulus delivery. On top, the topographic representation of amplitude distribution at …

https://doi.org/10.7554/eLife.09148.013
Figure 6 with 1 supplement
Representation of the physical design of electrodes for the hybrid model.

(a) Implementation for the TIME electrode. (b) Implementation for the microneedle. (c) Different locations for stimulating active site and tip, that were used in the model to compare the TIME …

https://doi.org/10.7554/eLife.09148.014
Figure 6—figure supplement 1
Finite element model development for the human median nerve, starting from histological pictures and resulting in the solution of voltage distribution within the nerve.
https://doi.org/10.7554/eLife.09148.015
Comparison of needle microstimulation and TIME stimulation using hybrid FEM/Neuron models.

(a,b), Recruitment curves of sensory axon populations resulting from different positions of the active sites for the needle microstimulation and TIME stimulation (mean +/- S.E.M. of percentage of …

https://doi.org/10.7554/eLife.09148.016
Figure 8 with 1 supplement
Fiber recruitment as a function of injected charge with microstimulation and the TIME implant.

(a) Recruitment results obtained for placement of the microneedle tip (insulated and non-insulated tip) and the TIME active site (L4 and R4) within the fascicle of interest. The recruitment curves …

https://doi.org/10.7554/eLife.09148.017
Figure 8—figure supplement 1
Representation of the 9 neural populations within large fascicles that were implemented in the hybrid electrical-biophysical model simulations to compare needle microstimulation and stimulation via implanted TIME interface.
https://doi.org/10.7554/eLife.09148.018
Subject behavior and analysis based on the stimulus spatial period (SP), inter-burst interval (IBI) and average firing rate (AFR) in the session with DAS amputee.

(a) Confusion matrix of the responses given by DAS subject. (b) Vertical bars display the correct responses, which are associated with each stimulus. The vertical solid lines over each bar indicate …

https://doi.org/10.7554/eLife.09148.019
Figure 10 with 1 supplement
Temporal coding of the spatial features of the experimented tactile stimuli.

In all panels the spatial structure (scale: 2 mm) of the grating is superimposed over a sample temporal pattern (scale: 200 ms) of the spike train that was obtained as a result of transduction with …

https://doi.org/10.7554/eLife.09148.020
Figure 10—figure supplement 1
Spatial modulation index that was calculated from the artificial-touch spike patterns from our study (left) compared to neurophysiological data shown by Phillips and Johnson for SA1 units (right, adapted from a previous study (Phillips and Johnson, 1981).

The depicted spatial modulations have the same monotonic trend versus the period of grating. The spatial modulation of our spike trains is globally higher in comparison with the neurophysiological …

https://doi.org/10.7554/eLife.09148.021
Author response image 1
Comparison of tactile neural sensory feedback techniques across literature.

Induced tactile sensations are classified as in a recent review (Saal and Bensmaia, 2015).

https://doi.org/10.7554/eLife.09148.022
Author response image 2
An example of the simulated stimulation of neural fibers by means of TIME interface, with the active site of the electrode close to, but outside from, the fascicle of interest (different populations are under-represented for the sake of proper visualization).
https://doi.org/10.7554/eLife.09148.023

Videos

Video 1
An example of the 3AFC psychophysical experiment with implanted intrafascicular stimulation of DAS amputee (as illustrated in Figure 1).

The video includes an interview with DAS amputee subject reporting the percepts immediately after one experimental session.

https://doi.org/10.7554/eLife.09148.006

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