Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation

Abstract

Pioneering work with nonhuman primates and recent human studies established intracortical microstimulation (ICMS) in primary somatosensory cortex (S1) as a method of inducing discriminable artificial sensation. However, these artificial sensations do not yet provide the breadth of cutaneous and proprioceptive percepts available through natural stimulation. In a tetraplegic human with two microelectrode arrays implanted in S1, we report replicable elicitations of sensations in both the cutaneous and proprioceptive modalities localized to the contralateral arm, dependent on both amplitude and frequency of stimulation. Furthermore, we found a subset of electrodes that exhibited multimodal properties, and that proprioceptive percepts on these electrodes were associated with higher amplitudes, irrespective of the frequency. These novel results demonstrate the ability to provide naturalistic percepts through ICMS that can more closely mimic the body's natural physiological capabilities. Furthermore, delivering both cutaneous and proprioceptive sensations through artificial somatosensory feedback could improve performance and embodiment in brain-machine interfaces.

Trial registration: ClinicalTrials.gov NCT01964261.

Keywords: brain-machine interface; human; intracortical microstimulation; neuroscience; proprioception; somatosensation; somatosensory cortex.

Figure 1.. Array implant locations on rendered MRI image of the left hemisphere of FG.

96-channel microelectrode arrays were implanted into ventral premotor cortex (PMv) and supramarginal gyrus (SMG), and two 48-channel stimulating arrays were implanted into primary somatosensory cortex (S1). The insert shows the in situ array locations.

Figure 2.. Receptive fields and sensation modality across all amplitude mapping experiments.

(A) Receptive field location on anterior (lighter shades) and posterior (darker shades) planes of the right upper arm (green), forearm (pink), and hand (cyan). Grid is the same that the subject referenced during the experiment. (B) Schematic of the two electrode arrays implanted over S1 (Figure 1). Left side panels display the reported receptive fields at each electrode location, and right side panels display the sensation modality (cutaneous - red, proprioceptive - blue). Light gray boxes show electrodes with no reported sensation, while dark gray boxes represent reference channels which are not used in recording. The five electrodes with a thick black outline represent the subset tested in the additional parameter-wide mapping task. Yellow and magenta asterisks mark the inferior-posterior corner of the implants, for the medial and lateral arrays respectively.

Figure 3.. Proprioceptive and cutaneous responses.

(A) Kernel density estimate and box plot showing the difference in the distribution of amplitudes associated with each report of proprioceptive (blue) or cutaneous (red) responses. (B) The median percentage of responses in the bootstrapped sample (solid line) for proprioceptive and cutaneous responses at each amplitude tested. Dashed line shows 1st-order polynomial fit. (C) Kernel density estimates of the distribution of slopes from 1st-order polynomial fits in each bootstrap iteration. (D) Pie charts show the percentage of total stimulations of responses for the subset of electrodes tested over a range of both current amplitudes and pulse frequencies. The left panel shows an individual example electrode (six trials per combination of amplitude and frequency) and the right panel shows data pooled over all five electrodes (30 total stimulations per combination). The percentage of no response (white), proprioceptive (blue) or cutaneous (red) are shown. (E) A normalized histogram of proprioceptive (blue) and cutaneous (red) responses at each of the amplitudes tested in experiment 2.