Visual inputs and postural manipulations affect the location of somatosensory percepts elicited by electrical stimulation

Abstract

The perception of somatosensation requires the integration of multimodal information, yet the effects of vision and posture on somatosensory percepts elicited by neural stimulation are not well established. In this study, we applied electrical stimulation directly to the residual nerves of trans-tibial amputees to elicit sensations referred to their missing feet. We evaluated the influence of congruent and incongruent visual inputs and postural manipulations on the perceived size and location of stimulation-evoked somatosensory percepts. We found that although standing upright may cause percept size to change, congruent visual inputs and/or body posture resulted in better localization. We also observed visual capture: the location of a somatosensory percept shifted toward a visual input when vision was incongruent with stimulation-induced sensation. Visual capture did not occur when an adopted posture was incongruent with somatosensation. Our results suggest that internal model predictions based on postural manipulations reinforce perceived sensations, but do not alter them. These characterizations of multisensory integration are important for the development of somatosensory-enabled prostheses because current neural stimulation paradigms cannot replicate the afferent signals of natural tactile stimuli. Nevertheless, multisensory inputs can improve perceptual precision and highlight regions of the foot important for balance and locomotion.

Figure 1

Three 16-contact C-FINEs were implanted around the sciatic, tibial, and common peroneal nerves of subject LL01 (left) and around the proximal sciatic, distal sciatic, and tibial nerves of subject LL02 (right). Reproduced from Charkhkar et al., (10.1088/1741-2552/aac964). © IOP Publishing Ltd. CC BY 3.0. Also printed with permission from © Novie Studio.

Figure 2

Experimental conditions are demonstrated by participant LL01. The number(s) in the left corner of each photo represent the condition number described in Table 1. The three photos in the bottom row have two numbers because each posture was repeated with the eyes open and closed.

Figure 3

Participant LL01 demonstrates the two supplemental static standing conditions. The number in the top left corner of each photo represents the condition number described in Table 1. When testing contacts F1 and F2, the eyes were open. For contacts R2 and R3, the eyes were closed.

Figure 4

During the baseline condition, each participant sat with the prosthesis elevated while an electrode contact delivered stimulation to the nerve. Participants then drew the perceived location of the evoked percept on a blank diagram of the intact foot and leg, represented here as one heat map per contact. Red areas indicate regions that were drawn in all fifteen trials. The forefoot region of interest (ROI) was classified as the primary ROI for contacts F1-F3, and the rearfoot ROI was classified as the primary ROI for contacts R1-R3.

Figure 5

A generic healthy foot is outlined in grey. Shaded red areas indicate regions that were reported more than the baseline condition, and shaded blue regions represent a decrease in reporting compared to baseline. The † symbol indicates significant changes in percept reporting frequency and/or percept size over the entire plantar surface of the foot (two-tailed paired t-tests, p < 0.05). (a) Stimulation was delivered while participants stood upright with their eyes closed. (b) Stimulation was delivered while participants stood upright with their eyes open, looking down at their feet.

Figure 6

A generic healthy foot is outlined in grey. Shaded red areas indicate regions that were reported more than the baseline condition, and shaded blue regions represent a decrease in reporting compared to baseline. The † symbol indicates significant changes in percept reporting frequency and/or percept size over the entire plantar surface of the foot (two-tailed paired t-tests, p < 0.05). We re-tested contacts F1, F2, R2, and R3 in two supplemental conditions. When testing contacts F1 and F2, the eyes were open in all three conditions shown here. For contacts R2 and R3, the eyes were closed. (a) During the “prosthesis off” condition, electrical stimulation was delivered while a participant stood upright without wearing a prosthesis. (b) During the “prosthesis unloaded” condition, electrical stimulation was delivered while a participant stood on a wooden box with the intact leg and let the prosthetic leg dangle in the air. (c) Electrical stimulation was delivered while participants stood upright with their prostheses loaded. These results are also shown in Fig. 5, but repeated here to easily identify perceptual differences between standing conditions.

Figure 7

Sensory detection thresholds while participants sat down with their prostheses elevated (teal) or stood upright with their eyes open (purple). N = 4 trials per contact per posture. The black bars indicate standard deviation.

Figure 8

A generic healthy foot is outlined in grey, and the location of an added input is outlined in black. “Congruent” signifies that the experimenter touched the location of the primary ROI. The forefoot contacts (F1-F3) had a primary ROI in the forefoot, and rearfoot contacts (R1-R3) had a primary ROI in the rearfoot. Shaded red areas indicate regions that were reported more than the baseline condition, and shaded blue regions represent a decrease in reporting compared to baseline. The † symbol denotes significantly increased activation in the primary ROI, and the ‡ symbol indicates significantly decreased activation in regions outside of the primary ROI (one-tailed paired t-tests, p < 0.05). (a) During the conditions involving congruent visual inputs, electrical stimulation was delivered while participants sat and watched an experimenter apply a light touch to the primary ROI on the plantar surface of the prosthesis. (b) During conditions involving congruent postural manipulations with the eyes closed, electrical stimulation was delivered while participants stood upright and adopted a posture that applied a load to the location of the primary ROI. (c) Repeated condition ‘b’ with the eyes open.

Figure 9

A generic healthy foot is outlined in grey, and the location of an added tactile input is outlined in black. “Incongruent” signifies that the experimenter touched a location outside of the primary ROI (forefoot contacts had a primary ROI in the forefoot, and rearfoot contacts had a primary ROI in the rearfoot). Shaded red areas indicate regions that were reported more than the baseline condition, and shaded blue regions represent a decrease in reporting compared to baseline. The † symbol denotes significantly increased activation in regions outside of the primary ROI, and the ‡ symbol indicates significantly decreased activation in the primary ROI (one-tailed paired t-tests, p < 0.05). (a) During the conditions involving incongruent visual inputs, electrical stimulation was delivered while participants sat and watched an experimenter apply a light touch to a region outside of the primary ROI. (b) During conditions involving incongruent postural manipulations with the eyes closed, electrical stimulation was delivered while participants stood upright and adopted a posture that applied a load away from the location of the primary ROI. (c) Repeated condition ‘b’ with the eyes open.