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Intracortical microstimulation pulse waveform and frequency recruits distinct spatiotemporal patterns of cortical neuron and neuropil activation

Kevin C. Stieger, James R. Eles, Kip A. Ludwig, View ORCID ProfileTakashi D.Y. Kozai
doi: https://doi.org/10.1101/2022.01.14.476351
Kevin C. Stieger
1Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA
2Center for the Neural Basis of Cognition, University of Pittsburgh, Carnegie Mellon University, Pittsburgh, PA
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James R. Eles
1Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA
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Kip A. Ludwig
3Department of Biomedical Engineering, University of Wisconsin Madison, Madison, Wisconsin
4Department of Neurological Surgery, University of Wisconsin Madison, Madison, Wisconsin
5Wisconsin Institute for Translational Neuroengineering (WITNe), Madison, Wisconsin, USA
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Takashi D.Y. Kozai
1Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA
2Center for the Neural Basis of Cognition, University of Pittsburgh, Carnegie Mellon University, Pittsburgh, PA
6Center for Neuroscience, University of Pittsburgh, Pittsburgh, PA
7McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA
8NeuroTech Center, University of Pittsburgh Brain Institute, Pittsburgh, PA
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  • ORCID record for Takashi D.Y. Kozai
  • For correspondence: tdk18@pitt.edu
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Abstract

Background Neural prosthetics often use intracortical microstimulation (ICMS) for sensory restoration. To restore natural and functional feedback, we must first understand how stimulation parameters influence the recruitment of neural populations. ICMS waveform asymmetry modulates the spatial activation of neurons around an electrode at 10 Hz; however, it is unclear how asymmetry may differentially modulate population activity at frequencies typically employed in the clinic (e.g. 100 Hz).

Objective We hypothesized that stimulation waveform asymmetry would differentially modulate preferential activation of certain neural populations, and the differential population activity would be frequency-dependent.

Methods We quantified how asymmetric stimulation waveforms delivered at 10 Hz or 100 Hz for 30s modulated spatiotemporal activity of cortical layer II/III pyramidal neurons using in vivo two-photon and mesoscale calcium imaging in anesthetized mice. Asymmetry is defined in terms of the ratio of the leading phase to the return phase of charge-balanced cathodal- and anodal-first waveforms.

Results Neurons within 40-60μm of the electrode display stable stimulation-induced activity indicative of direct activation, which was independent of waveform asymmetry. The stability of 72% of activated neurons and the preferential activation of 20-90 % of neurons depended on waveform asymmetry. Additionally, this asymmetry-dependent activation of different neural populations was associated with differential progression of population activity. Specifically, neural activity increased over time for some waveforms at 10 Hz, but decreased more at 100 Hz than other waveforms.

Conclusion These data demonstrate that at frequencies commonly used for sensory restoration, stimulation waveform alters the pattern of activation of different but overlapping populations of excitatory neurons. The impact of these waveform specific responses on the activation of different subtypes of neurons as well as sensory perception merits further investigation.

Competing Interest Statement

The authors declare no competing interests. KAL is a scientific board member and has stock interests in NeuroOne Medical Inc., a company developing next generation epilepsy monitoring devices. KAL is also paid member of the scientific advisory board of Cala Health, Blackfynn, Abbott and Battelle. KAL also is a paid consultant for Galvani and Boston Scientific. KAL is a consultant to and co-founder of Neuronoff Inc. None of these associations are directly relevant to the work presented in this manuscript.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted January 17, 2022.
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Intracortical microstimulation pulse waveform and frequency recruits distinct spatiotemporal patterns of cortical neuron and neuropil activation
Kevin C. Stieger, James R. Eles, Kip A. Ludwig, Takashi D.Y. Kozai
bioRxiv 2022.01.14.476351; doi: https://doi.org/10.1101/2022.01.14.476351
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Intracortical microstimulation pulse waveform and frequency recruits distinct spatiotemporal patterns of cortical neuron and neuropil activation
Kevin C. Stieger, James R. Eles, Kip A. Ludwig, Takashi D.Y. Kozai
bioRxiv 2022.01.14.476351; doi: https://doi.org/10.1101/2022.01.14.476351

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