• Figure 1.
    Download figureOpen in new tabFigure 1. 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 spike trains that were generated in all sessions with one subject by the artificial finger while the gratings were slid. (c) Setup of percutaneous electrical microstimulation (left) and implanted intrafascicular stimulation (right) of the median nerve, and discrimination performance during all experimental sessions involving four intact subjects and one transradial upper limb amputee.Source data of the spike trains that were transduced by the artificial finger while the gratings were indented and slid over have been deposited in Dryad (Oddo et al., 2016). Such spikes were used to trigger the neural stimulator in all the experimental sessions with DAS amputee (raster plot depicted in Figure 1b).

    DOI: http://dx.doi.org/10.7554/eLife.09148.003

    Figure 2.
    Download figureOpen in new tabFigure 2. 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), grating with ridges and grooves that alternate with spatial period SP, and sensorized fingertip, which is in contact with tactile stimulus. (b) The sequence of presentation of surface pair to the artificial finger. (c) Example of implementation of the Izhikevich model for real-time conversion of MEMS sensor data into a sequence of artificial neural spikes. The blue and green traces show raw sensor outputs from the pair of opposing channels depicted in panel a. The red trace shows the input to the Izhikevich artificial neuron, which results from the application of Equation 1 and 2 (described in the Materials and methods section). The black lines depict the spikes that are generated when the membrane potential of the Izhikevich artificial neuron reaches the threshold (Equation 5 in the Materials and methods section) and, thus, the neural stimulator is triggered. (d–e) Implementation of the Izhikevich model with a close-up view during the sliding motion over the first and second halves of the grating. The traces and color-coding are shown in panel c.

    DOI: http://dx.doi.org/10.7554/eLife.09148.004

    Figure 3.
    Download figureOpen in new tabFigure 3. 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 microstimulation. The titles indicate correct/total responses (percentage). (b) Vertical bars display correct responses that are associated with each stimulus. The vertical solid lines over each bar indicate the 95% confidence intervals (Clopper Pearson exact interval) per stimulus. The dashed horizontal line indicates chance level (1/3). (c) The fraction of trials a pair of stimuli is perceived as different as a function of difference in spatial period (ΔSP) between the two stimulus halves, and logistic fit (dashed line). The title reports the R2 associated with the fit, i.e., the fraction of data variance explained by the logistic function, and the significance of the Pearson correlation between data points and the fit.

    DOI: http://dx.doi.org/10.7554/eLife.09148.005

    Figure 5.
    Download figureOpen in new tabFigure 5. 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 different time lags (ms). (b) Position of the associated equivalent dipole, which corresponds to P27 peak, superimposed on the individual horizontal, coronal and sagittal structural MRI planes of the subject.

    DOI: http://dx.doi.org/10.7554/eLife.09148.013

    Figure 7.
    Download figureOpen in new tabFigure 7. 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 recruited fibers). R4/L4 is the pair of active sites within the target fascicle; R5/L5 is close to it, and R6/L6 is shielded with respect to it. For each position of the stimulating tip/active site, nine different axonal populations were computed. The fiber was considered active when the spike travelled until the last node of Ranvier that was implemented. Figure insets represent voltage distributions for different positions of active sites, as calculated using the FEM solver. These results are representative for several electrode insertion configurations. The same computations were performed for medium and small fascicles and confirmed the results.

    DOI: http://dx.doi.org/10.7554/eLife.09148.016

    Figure 9.
    Download figureOpen in new tabFigure 9. 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 the 95% confidence intervals (Clopper Pearson exact interval) per stimulus. The dashed horizontal line indicates chance level (1/3). (c) Fraction of trials for which a pair of stimuli is perceived as different as a function of the difference in spatial period (ΔSP) between the two stimulus halves, and logistic fit (dashed line). The title reports the R2 associated with the fit, i.e., the fraction of data variance explained by the logistic function, and the significance of the Pearson correlation between data points and the fit. (d,e) Comparison between IBI-based and AFR-based discrimination. Difference between IBIs (ΔIBI, panel d) and difference between AFRs (ΔAFR, panel e) measured in the spike patterns elicited by the two sides of each stimulus and plotted as a function of the difference between grating SPs (ΔSP). Error bars indicate the interquartile range. The title reports the fraction of explained variance.

    DOI: http://dx.doi.org/10.7554/eLife.09148.019

  • 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.

    DOI: http://dx.doi.org/10.7554/eLife.09148.006

  • The following dataset was generated:

    Oddo CM, Raspopovic S, Artoni F, Mazzoni A, Spigler G, Petrini F, Federica G, Fabrizio V, Francesca M, Loredana Z, Di Pino G, Camboni D, Carrozza MC, Guglielmelli E, Rossini PM, Faraguna U, Micera S, 2015,Data from Intraneural stimulation elicits discrimination of textural features by artificial fingertip in intact and amputee humans, http://dx.doi.org/10.5061/dryad.630hf, Available at Dryad Digital Repository under a CC0 Public Domain Dedication