Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 110 (45), 18279-84

Restoring the Sense of Touch With a Prosthetic Hand Through a Brain Interface

Affiliations

Restoring the Sense of Touch With a Prosthetic Hand Through a Brain Interface

Gregg A Tabot et al. Proc Natl Acad Sci U S A.

Abstract

Our ability to manipulate objects dexterously relies fundamentally on sensory signals originating from the hand. To restore motor function with upper-limb neuroprostheses requires that somatosensory feedback be provided to the tetraplegic patient or amputee. Given the complexity of state-of-the-art prosthetic limbs and, thus, the huge state space they can traverse, it is desirable to minimize the need for the patient to learn associations between events impinging on the limb and arbitrary sensations. Accordingly, we have developed approaches to intuitively convey sensory information that is critical for object manipulation--information about contact location, pressure, and timing--through intracortical microstimulation of primary somatosensory cortex. In experiments with nonhuman primates, we show that we can elicit percepts that are projected to a localized patch of skin and that track the pressure exerted on the skin. In a real-time application, we demonstrate that animals can perform a tactile discrimination task equally well whether mechanical stimuli are delivered to their native fingers or to a prosthetic one. Finally, we propose that the timing of contact events can be signaled through phasic intracortical microstimulation at the onset and offset of object contact that mimics the ubiquitous on and off responses observed in primary somatosensory cortex to complement slowly varying pressure-related feedback. We anticipate that the proposed biomimetic feedback will considerably increase the dexterity and embodiment of upper-limb neuroprostheses and will constitute an important step in restoring touch to individuals who have lost it.

Keywords: brain-computer interface; brain-machine interface; macaque.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Experimental design. (A, Upper) Trial structure for all of the behavioral tasks: The cross is a fixation target or a response target, and the yellow circles indicate the two stimulus intervals. (A, Lower) One example trial each for the location discrimination and the pressure discrimination task. The size of the cross is proportional to the depth of indentation. (B) Depiction of the triaxial indenting stimulator. (Upper Inset) Trajectory of the tactile stimuli, which consisted of 1-s-long trapezoidal indentations into the skin. (Lower Inset) Structure of ICMS, which consisted of 300-Hz trains of symmetric biphasic pulses (phase duration = 200 µs, interphase duration = 53 µs) (38) lasting 1 s unless otherwise specified. (C) Chronic electrode implants in one of the three animals, showing the UEA, impinging on area 1, flanked by two FMAs, impinging on area 3b. We used FMAs to target area 3b, because the digit representation of area 3b is located deep in the posterior bank of the central sulcus and cannot be accessed with the 1.5-mm-long UEA electrodes. The UEA and the lateral-anterior FMA impinged on the hand representation; the medial-posterior FMA impinged on the arm representation in all three animals and so it was not used in the experiments. (D) RF map of the UEA and the lateral-anterior FMA. The UEA in this animal had RFs on the palm and digits 3–5; the FMA had RFs primarily on digit 2 (index). A red X denotes a reference electrode.
Fig. 2.
Fig. 2.
Localization performance was similar with mechanical touch and ICMS. (A) On both mechanical and hybrid trials, the relative locations of stimuli applied to widely spaced digits were more accurately discriminated than were the relative locations of stimuli applied to adjacent digits. Measured from one animal, mechanical performance was based on 1,160 and 1,031 trials, respectively (green and gold); hybrid performance on 246 and 196 trials, respectively. To compare performance on hybrid trials and performance on mechanical trials matched for hand location, we computed the difference between the two: ΔP = pmech(correct) − phybrid(correct). (B) Performance on mechanical and hybrid trials was nearly equivalent. Shown is the distribution of Δp for the two animals tested on this task (132 stimulus pairs, 27 different electrodes, 16 of which are UEAs). Across electrodes, performance was significantly above chance, demonstrating that ICMS yields spatially localized percepts. Performance on hybrid trials was somewhat lower than on mechanical location discrimination trials (median ΔP = 0.056), suggesting that the elicited percepts may be somewhat more diffuse than natural ones. There was no significant difference in performance based on stimulation of areas 3b or 1, so data from these two areas are pooled.
Fig. 3.
Fig. 3.
Information about contact pressure was conveyed by varying ICMS amplitude. (A) Detection of ICMS in areas 3b and 1 followed a sigmoidal relationship to amplitude, shown here for one animal (area 3b: 19,184 trials, 7 electrodes; area 1: 29,498 trials, 27 electrodes). The horizontal dashed line indicates the threshold criterion. (Inset) Distribution of detection thresholds (75% detection) for all three animals (area 3b: 19 electrodes; area 1: 35 electrodes). There were no significant differences in sensitivity to ICMS across animals or anatomical areas. (B) ICMS amplitude was a power function of mechanical amplitude matched in perceived magnitude. Shown are PEFs derived from all of the electrodes for which there were both detection and discrimination data. Mechanical data from the electrode’s RF was used to generate the function. The two colors correspond to two different monkeys with 4 and 12 electrodes (the third did not perform the discrimination task so did not yield PEFs). The darker traces show the pooled PEFs for each monkey. The equations are for the power functions fit to the pooled PEFs for the two monkeys are shown. (C) Discriminability of stimulus amplitude is equivalent when mechanical indentations are applied to the animal’s own finger (blue) or to a prosthetic finger and converted to ICMS (red) (two animals with 240 and 360 trials with the prosthetic finger and 1,120 trials with the native finger). The mapping between time-varying pressure and time-varying ICMS amplitude was achieved by using the PEF. See Fig. S4 for analogous results in a detection task.
Fig. 4.
Fig. 4.
(A) Animals are able to compare mechanical indentations to ICMS pulse trains scaled by using PEFs. The monkey compared a standard mechanical stimulus of fixed amplitude to a comparison electrical stimulus of variable amplitude (ranging from 20 to 80 µA) (performance pooled over 4 electrodes, 2 UEAs, and 2 FMAs for a total of 4,114 trials). The amplitude of the standard was matched in subjective magnitude with an electrical stimulus of amplitude 50 µA based on the PEF of each electrode tested (mean amplitude = 440 µm, range 200–750 µm). The animal judged which of the two stimuli was stronger, demonstrating that it could compare mechanical and electrical stimuli along a single perceptual dimension (magnitude). Error bars denote the SEM. (B) Sensitivity to ICMS increases with duration up to ∼100 ms. Thresholds decrease as duration increases from 50 to 100 ms then level off. Thus, a 100-ms pulse at 80 µA will be clearly perceptible and can be used to signal the onset and offset of contact, mimicking the onset and offset responses observed in the somatosensory cortex of intact individuals. Error bars denote the SEM. These functions show the mean performance across four electrodes in area 3b in one animal.

Similar articles

See all similar articles

Cited by 65 PubMed Central articles

See all "Cited by" articles

Publication types

LinkOut - more resources

Feedback