Temporal patterns in electrical nerve stimulation: Burst gap code shapes tactile frequency perception

Ng, Kevin K. W.; Olausson, Christoffer; Vickery, Richard M.; Birznieks, Ingvars

doi:10.1371/journal.pone.0237440

Cited by 16 publications

(13 citation statements)

References 60 publications

(87 reference statements)

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“…The mean equivalent tactile perceived frequency for stimulus DA25 was 27.0 Hz (95% CI: 25.3-28.8), for stimulus DA50 was 47.9 Hz (45.0-50.8) and stimulus DA100 was 90.9 Hz (81.9-99.8). Although these values are close to their burst-gap model predicted values depicted by the dashed lines [which correspond to the reciprocal of the inter-burst interval in the test train (Birznieks and Vickery, 2017;Ng et al, 2020Ng et al, , 2021], the data for DA25 and DA100 differed from the predicted values of 25 Hz (p = 0.029, n = 12, one-sample t-test) and 100 Hz (p = 0.047, n = 12, onesample t-test); while for stimulus DA50, there was no statistical difference from the burst-gap predicted value (50 Hz, p = 0.13, n = 12). However, the data for DA25 and DA100 was much more poorly predicted by their periodicity (23 Hz, p = 0.0004; and 67 Hz, p = 0.0001; one-sample t-test) or mean pulse rate (46 Hz, p < 0.0001; and 134 Hz, p < 0.0001) than from burstgap predictions, suggesting the burst-gap model offers a better explanation.…”

Section: Perceptual Equivalence Between Cross-modal Bursting and Regu...supporting

confidence: 65%

“…The inter-burst intervals in test trains were set at 40, 20, and 10 ms to correspond to expected perceived frequencies of 25, 50, and 100 Hz, respectively, for the doublet acoustic (DA25, DA50, and DA100) (Sharma et al, 2022) and vibrotactile (DT25, DT50, and DT100) test trains (Ng et al, 2020). The cross-modal regular comparisons that spanned 12-44, 24-88, and 48-176 Hz for stimuli DA/DT25-100, respectively, were identical to experiment 1, regardless of sensory modality used for the comparison.…”

Section: Experiments 2: Doublet Burst Patternsmentioning

confidence: 99%

“…In these experiments, we first tested stimuli spanning the flutter and vibratory hum range in their simplest form (regular acoustic and vibrotactile pulse trains). Second, we compared stimuli organised as bursts of pulses in one modality with regular stimuli in the other, with the hypothesis that the frequency of the matching regular pulse train will equal that predicted from the inter-burst gap, as previously shown in unimodal studies (Birznieks and Vickery, 2017;Ng et al, 2020Ng et al, , 2021Sharma et al, 2022). The pulsatile stimulation technique employed in this study allows precise control of the timing of spikes in a fixed population of primary afferents responding to the stimulus modality.…”

Section: Introductionmentioning

confidence: 99%

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Auditory clicks elicit equivalent temporal frequency perception to tactile pulses: A cross-modal psychophysical study

Sharma

Birznieks

et al. 2022

Front. Neurosci.

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Both hearing and touch are sensitive to the frequency of mechanical oscillations—sound waves and tactile vibrations, respectively. The mounting evidence of parallels in temporal frequency processing between the two sensory systems led us to directly address the question of perceptual frequency equivalence between touch and hearing using stimuli of simple and more complex temporal features. In a cross-modal psychophysical paradigm, subjects compared the perceived frequency of pulsatile mechanical vibrations to that elicited by pulsatile acoustic (click) trains, and vice versa. Non-invasive pulsatile stimulation designed to excite a fixed population of afferents was used to induce desired temporal spike trains at frequencies spanning flutter up to vibratory hum (>50 Hz). The cross-modal perceived frequency for regular test pulse trains of either modality was a close match to the presented stimulus physical frequency up to 100 Hz. We then tested whether the recently discovered “burst gap” temporal code for frequency, that is shared by the two senses, renders an equivalent cross-modal frequency perception. When subjects compared trains comprising pairs of pulses (bursts) in one modality against regular trains in the other, the cross-sensory equivalent perceptual frequency best corresponded to the silent interval between the successive bursts in both auditory and tactile test stimuli. These findings suggest that identical acoustic and vibrotactile pulse trains, regardless of pattern, elicit equivalent frequencies, and imply analogous temporal frequency computation strategies in both modalities. This perceptual correspondence raises the possibility of employing a cross-modal comparison as a robust standard to overcome the prevailing methodological limitations in psychophysical investigations and strongly encourages cross-modal approaches for transmitting sensory information such as translating pitch into a similar pattern of vibration on the skin.

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Section: Perceptual Equivalence Between Cross-modal Bursting and Regu...supporting

confidence: 65%

Section: Experiments 2: Doublet Burst Patternsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Auditory clicks elicit equivalent temporal frequency perception to tactile pulses: A cross-modal psychophysical study

Sharma

Birznieks

et al. 2022

Front. Neurosci.

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“…This is surprising in light of the fact that nonhuman primates can distinguish the PF of intracortical microstimulation up to ∼200 Hz, though sensitivity to changes in PF decreases at high frequencies ( Callier et al, 2020 ). While prior studies of electrocutaneous stimulation reported discriminability of pulse trains up to 100 Hz ( Anani et al, 1977 ; Szeto et al, 1979 ; Ng et al, 2020 , 2021 ), the psychophysical tasks in these prior studies were not designed to eliminate intensity cues; so, results therefrom are difficult to compare with those reported here. Indeed, intensity discrimination of direct nerve stimulation has also been observed up to 100 Hz ( Graczyk et al, 2016 ).…”

Section: Discussionmentioning

confidence: 74%

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

Graczyk

Christie

et al. 2022

J. Neurosci.

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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.

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“…Considering two successive isolated pulses, the minimal interval is about 40 ms 41 , whereas with pulse trains, the limit between the flutter range (discrete events) and the continuous vibration range was evaluated at 60 Hz ( 15 ms intervals) 15 , 42 . This value has been verified using both periodic 43 , 44 and aperiodic 45 stimuli: the authors showed that the tactile sensation of frequency is determined by the duration of the silence intervals between the pulses. Intervals longer than 15 ms are crucial whereas shorter intervals have only a limited effect on the frequency evaluation, exhibiting the limit of the discrete perception below this value.…”

Section: Discussionmentioning

confidence: 78%

Rhythm perception is shared between audio and haptics

Bernard

Monnoyer

Wiertlewski

et al. 2022

Sci Rep

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A surface texture is perceived through both the sound and vibrations produced while being explored by our fingers. Because of their common origin, both modalities have a strong influence on each other, particularly at above 60 Hz for which vibrotactile perception and pitch perception share common neural processes. However, whether the sensation of rhythm is shared between audio and haptic perception is still an open question. In this study, we show striking similarities between the audio and haptic perception of rhythmic changes, and demonstrate the interaction of both modalities below 60 Hz. Using a new surface-haptic device to synthesize arbitrary audio-haptic textures, psychophysical experiments demonstrate that the perception threshold curves of audio and haptic rhythmic gradients are the same. Moreover, multimodal integration occurs when audio and haptic rhythmic gradients are congruent. We propose a multimodal model of rhythm perception to explain these observations. These findings suggest that audio and haptic signals are likely to be processed by common neural mechanisms also for the perception of rhythm. They provide a framework for audio-haptic stimulus generation that is beneficial for nonverbal communication or modern human-machine interfaces.

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Temporal patterns in electrical nerve stimulation: Burst gap code shapes tactile frequency perception

Cited by 16 publications

References 60 publications

Auditory clicks elicit equivalent temporal frequency perception to tactile pulses: A cross-modal psychophysical study

Auditory clicks elicit equivalent temporal frequency perception to tactile pulses: A cross-modal psychophysical study

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

Rhythm perception is shared between audio and haptics

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