Frequency Shapes the Quality of Tactile Percepts Evoked through Electrical Stimulation of the Nerves

Abstract

Electrical stimulation of the peripheral nerves of human participants provides a unique opportunity to study the neural determinants of perceptual quality using a causal manipulation. A major challenge in the study of neural coding of touch has been to isolate the role of spike timing -at the scale of milliseconds or tens of milliseconds -in shaping the sensory experience.In the present study, we address this question by systematically varying the frequency (PF) of electrical stimulation pulse trains delivered to the peripheral nerves of seven participants with upper and lower extremity limb loss via chronically implanted neural interfaces. We find that increases in PF lead to systematic increases in perceived frequency, up to about 50 Hz, at which point further changes in PF have little to no impact on sensory quality. Above this transition frequency, ratings of perceived frequency level off, the ability to discriminate changes in PF is abolished, and verbal descriptors selected to characterize the sensation change abruptly. We conclude that sensation quality is shaped by temporal patterns of neural activation, even if these patterns are imposed on a fixed neural population, but this temporal patterning can only be resolved up to about 50 Hz. These findings highlight the importance of spike timing in shaping the quality of a sensation and will contribute to the development of encoding strategies for conveying touch feedback through bionic hands and feet. SIGNIFICANCE STATEMENTA major challenge in the study of neural coding of touch has been to understand how temporal patterns in neuronal responses shape the sensory experience. We address this question by varying the frequency (PF) of electrical pulse trains delivered through implanted nerve interfaces in seven amputees. We concomitantly vary pulse width to separate the effect of changing PF on sensory quality from its effect on perceived magnitude. We find that increases in PF lead to increases in perceived frequency, a qualitative dimension, up to about 50Hz, beyond which changes in PF have little impact on quality. We conclude that temporal patterning in the neuronal response can shape quality and discuss the implications for restoring touch via neural interfaces.

The experience of sensorimotor integration of a lower limb sensory neuroprosthesis: A qualitative case study

“…As expected from prior psychometric studies of sensory stimulation ( Graczyk et al, 2016 , 2022 ; Charkhkar et al, 2018 ), the sensation modality and intensity depended strongly on the stimulation levels set by the participant. When the stimulation levels were low, the participant described the stimulation-elicited sensations as “tingly” or “a very light tingling.” When the stimulation levels were high, the participant explained how the sensation modality changed:…”

How Fast Is Too Fast? Boundaries to the Perception of Electrical Stimulation of Peripheral Nerves

“…Similarly, George et al [17] showed that intensity discrimination was better at lower f s (12.5 -87.5 Hz) than higher frequencies (50 -200 Hz). A recent study into the influence of intraneural stimulation frequency and pulse width found that participants were able to discriminate frequencies in the range of 2 -∼50 Hz, but that ability broke down beyond a stimulus frequency of 60 Hz [41]. One other study including f s up to 500 Hz did find a linear relationship between f s and perception magnitude [9].…”

Perceived Timing of Cutaneous Vibration and Intracortical Microstimulation of Human Somatosensory Cortex

“…None of the electrodes in any of the participant’s arrays elicited an ICMS sensation that was described as resembling vibration in prior characterization experiments, even when testing a variety of stimulation parameters. Only a few recent studies have started to systematically characterize the relationship between stimulation parameters and the perceived quality of artificial touch [25], [39]. When future technology enables us to selectively activate specific neurons in somatosensory cortex, likely creating more natural-feeling percepts, it would be interesting to repeat these tests.…”