A biomimetic electrical stimulation strategy to induce asynchronous stochastic neural activity

Formento, Emanuele; D’Anna, Edoardo; Gribi, Sandra; Lacour, Stéphanie; Micera, Silvestro

doi:10.1088/1741-2552/aba4fc

Cited by 32 publications

(26 citation statements)

References 45 publications

(70 reference statements)

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“…Pulsed electrical stimulation of the nerve also produces a highly periodic response in the activated tactile nerve fibers ( Formento et al, 2020 ), and this frequency-dependent temporal patterning likely mediates the ability to discriminate the perceived frequency of electrical pulse trains. In fact, sensitivity to changes in the frequency of electrical stimulation is similar to its vibrotactile counterpart, both yielding Weber fractions of ∼0.2.…”

Section: Discussionmentioning

confidence: 99%

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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Section: Discussionmentioning

confidence: 99%

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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“…Indeed, biologically occurring neural activity usually follows a much more desynchronized pattern with a firing frequency modelled as a Poisson point process (Johnson & Hsiao, 1992). Interestingly with the modulation of multiple stimulation parameters, Formento et al (2020) proposed a novel stimulation scheme (i.e., BioS) designed to desynchronize the neural activity induced by electrical stimulation (validated in silico and in vitro), potentially allowing future biomimetic encoding strategies to replicate natural patterns of activity with even higher fidelity.…”

Section: Biomimicry As Fundamental Feature For Neurostimulation Designmentioning

confidence: 99%

Peripheral neurostimulation for encoding artificial somatosensations

Valle

2022

Eur J of Neuroscience

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The direct neural stimulation of peripheral or central nervous systems has been shown as an effective tool to treat neurological conditions. The electrical activation of the nervous sensory pathway can be adopted to restore the artificial sense of touch and proprioception in people suffering from sensory‐motor disorders. The modulation of the neural stimulation parameters has a direct effect on the electrically induced sensations, both when targeting the somatosensory cortex and the peripheral somatic nerves. The properties of the artificial sensations perceived, as their location, quality and intensity are strongly dependent on the direct modulation of pulse width, amplitude and frequency of the neural stimulation. Different sensory encoding schemes have been tested in patients showing distinct effects and outcomes according to their impact on the neural activation. Here, I reported the most adopted neural stimulation strategies to artificially encode somatosensation into the peripheral nervous system. The real‐time implementation of these strategies in bionic devices is crucial to exploit the artificial sensory feedback in prosthetics. Thus, neural stimulation becomes a tool to directly communicate with the human nervous system. Given the importance of adding artificial sensory information to neuroprosthetic devices to improve their control and functionality, the choice of an optimal neural stimulation paradigm could increase the impact of prosthetic devices on the quality of life of people with sensorimotor disabilities.

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“…In the spinal manifold, firing rates projected robust and closed trajectories in response to proprioceptive stimuli. Obviously, the robustness of our trajectories across animals stems from the fact that we produced artificial proprioceptive stimuli using electrical stimulation of the peripheral nerves, which produces strong synchronized volleys of activity rather than asynchronous burst of inputs 45,46 . Nevertheless, their reproducibility allowed us to appreciate quantitative changes in shape and features occurring at various conditions, i.e., reduced proprioceptive input or concurrent stimulation of cutaneous afferents.…”

Section: Analysis Of Neural Manifolds Reveals Disruption Of Intra-spinal Processing Of Proprioceptive Informationmentioning

confidence: 99%

Neural population dynamics reveals disruption of spinal sensorimotor computations during electrical stimulation of sensory afferents

Katic

Balaguer

Gorskii

et al. 2021

Preprint

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Restoration of proprioception with neurotechnology is critical to improve effectiveness of robotic neuro-prostheses. Unfortunately, after initial enthusiasm clinical results showed that unlike touch, proprioception could not be reliably induced. Here we show that concurrent activation of multiple sensory modalities may trigger unwanted sensory regulation mechanisms that disrupt proprioception. We recorded intra-spinal neural activity induced by stimulation of proprioceptive afferents from the radial nerve in three monkeys. Then, we superimposed stimulation of the radial nerve cutaneous branch and quantified its impact on spinal neural activity via population analysis. Proprioceptive pulses produced robust neural trajectories in the neural manifold that were disrupted by concurrent stimulation of cutaneous afferents. This disruption correlated with a reduction of afferent volleys and multi-unit activity both in the spinal cord and somatosensory cortex. Our results suggest that limited specificity not only impacts localization of artificial percepts, but also their nature to an extent that was never considered.

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A biomimetic electrical stimulation strategy to induce asynchronous stochastic neural activity

Cited by 32 publications

References 45 publications

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

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

Peripheral neurostimulation for encoding artificial somatosensations

Neural population dynamics reveals disruption of spinal sensorimotor computations during electrical stimulation of sensory afferents

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