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Low-threshold, high-resolution, chronically stable intracortical microstimulation by ultraflexible electrodes.

ABSTRACT: Intracortical microstimulation (ICMS) enables applications ranging from neuroprosthetics to causal circuit manipulations. However, the resolution, efficacy, and chronic stability of neuromodulation are often compromised by adverse tissue responses to the indwelling electrodes. Here we engineer ultraflexible stim-nanoelectronic threads (StimNETs) and demonstrate low activation threshold, high resolution, and chronically stable ICMS in awake, behaving mouse models. In vivo two-photon imaging reveals that StimNETs remain seamlessly integrated with the nervous tissue throughout chronic stimulation periods and elicit stable, focal neuronal activation at low currents of 2 μA. Importantly, StimNETs evoke longitudinally stable behavioral responses for over 8 months at a markedly low charge injection of 0.25 nC/phase. Quantified histological analyses show that chronic ICMS by StimNETs induces no neuronal degeneration or glial scarring. These results suggest that tissue-integrated electrodes provide a path for robust, long-lasting, spatially selective neuromodulation at low currents, which lessens risk of tissue damage or exacerbation of off-target side effects.

SUBMITTER: Lycke R

PROVIDER: S-EPMC10592461 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Low-threshold, high-resolution, chronically stable intracortical microstimulation by ultraflexible electrodes.

Lycke Roy R Kim Robin R Zolotavin Pavlo P Montes Jon J Sun Yingchu Y Koszeghy Aron A Altun Esra E Noble Brian B Yin Rongkang R He Fei F Totah Nelson N Xie Chong C Luan Lan L

Cell reports 20230524 6

Intracortical microstimulation (ICMS) enables applications ranging from neuroprosthetics to causal circuit manipulations. However, the resolution, efficacy, and chronic stability of neuromodulation are often compromised by adverse tissue responses to the indwelling electrodes. Here we engineer ultraflexible stim-nanoelectronic threads (StimNETs) and demonstrate low activation threshold, high resolution, and chronically stable ICMS in awake, behaving mouse models. In vivo two-photon imaging revea ...[more]

PMID: 37235473

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Project description:Objective.Persons with tetraplegia can use brain-machine interfaces to make visually guided reaches with robotic arms. Without somatosensory feedback, these movements will likely be slow and imprecise, like those of persons who retain movement but have lost proprioception. Intracortical microstimulation (ICMS) has promise for providing artificial somatosensory feedback. ICMS that mimics naturally occurring neural activity, may allow afferent interfaces that are more informative and easier to learn than stimulation evoking unnaturalistic activity. To develop such biomimetic stimulation patterns, it is important to characterize the responses of neurons to ICMS.Approach.Using a Utah multi-electrode array, we recorded activity evoked by both single pulses and trains of ICMS at a wide range of amplitudes and frequencies in two rhesus macaques. As the electrical artifact caused by ICMS typically prevents recording for many milliseconds, we deployed a custom rapid-recovery amplifier with nonlinear gain to limit signal saturation on the stimulated electrode. Across all electrodes after stimulation, we removed the remaining slow return to baseline with acausal high-pass filtering of time-reversed recordings.Main results.After single pulses of stimulation, we recorded what was likely transsynaptically-evoked activity even on the stimulated electrode as early as ∼0.7 ms. This was immediately followed by suppressed neural activity lasting 10-150 ms. After trains, this long-lasting inhibition was replaced by increased firing rates for ∼100 ms. During long trains, the evoked response on the stimulated electrode decayed rapidly while the response was maintained on non-stimulated channels.Significance.The detailed description of the spatial and temporal response to ICMS can be used to better interpret results from experiments that probe circuit connectivity or function of cortical areas. These results can also contribute to the design of stimulation patterns to improve afferent interfaces for artificial sensory feedback.

Dataset Information

Low-threshold, high-resolution, chronically stable intracortical microstimulation by ultraflexible electrodes.

Publications

Low-threshold, high-resolution, chronically stable intracortical microstimulation by ultraflexible electrodes.

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