Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array

Dongxiao Yan; Ahmad A. Jiman; Elizabeth C. Bottorff; Paras R. Patel; Dilara Meli; Elissa J. Welle; David C. Ratze; Leif A. Havton; Cynthia A. Chestek; Stephen W.P. Kemp; Tim M. Bruns; Euisik Yoon; John P. Seymour

doi:10.1002/smll.202200311

Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array

Dongxiao Yan, Ahmad A. Jiman, Elizabeth C. Bottorff, Paras R. Patel, Dilara Meli, Elissa J. Welle, David C. Ratze, Leif A. Havton, Cynthia A. Chestek, Stephen W.P. Kemp, Tim M. Bruns, Euisik Yoon, John P. Seymour

Yonsei Advanced Science Institute

Research output: Contribution to journal › Article › peer-review

4 Citations (Scopus)

Abstract

Peripheral nerve mapping tools with higher spatial resolution are needed to advance systems neuroscience, and potentially provide a closed-loop biomarker in neuromodulation applications. Two critical challenges of microscale neural interfaces are 1) how to apply them to small peripheral nerves, and 2) how to minimize chronic reactivity. A flexible microneedle nerve array (MINA) is developed, which is the first high-density penetrating electrode array made with axon-sized silicon microneedles embedded in low-modulus thin silicone. The design, fabrication, acute recording, and chronic reactivity to an implanted MINA, are presented. Distinctive units are identified in the rat peroneal nerve. The authors also demonstrate a long-term, cuff-free, and suture-free fixation manner using rose bengal as a light-activated adhesive for two time-points. The tissue response is investigated at 1-week and 6-week time-points, including two sham groups and two MINA-implanted groups. These conditions are quantified in the left vagus nerve of rats using histomorphometry. Micro computed tomography (micro-CT) is added to visualize and quantify tissue encapsulation around the implant. MINA demonstrates a reduction in encapsulation thickness over previously quantified interfascicular methods. Future challenges include techniques for precise insertion of the microneedle electrodes and demonstrating long-term recording.

Original language	English
Article number	2200311
Journal	Small
Volume	18
Issue number	21
DOIs	https://doi.org/10.1002/smll.202200311
Publication status	Published - 2022 May 26

Bibliographical note

Funding Information:
The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro-CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro-CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth.

Funding Information:
The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro‐CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro‐CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1 ). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth.

Publisher Copyright:
© 2022 Wiley-VCH GmbH.

All Science Journal Classification (ASJC) codes

Biotechnology
Biomaterials
Chemistry(all)
Materials Science(all)

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10.1002/smll.202200311

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Yan, D., Jiman, A. A., Bottorff, E. C., Patel, P. R., Meli, D., Welle, E. J., Ratze, D. C., Havton, L. A., Chestek, C. A., Kemp, S. W. P., Bruns, T. M., Yoon, E., & Seymour, J. P. (2022). Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array. Small, 18(21), [2200311]. https://doi.org/10.1002/smll.202200311

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title = "Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array",

abstract = "Peripheral nerve mapping tools with higher spatial resolution are needed to advance systems neuroscience, and potentially provide a closed-loop biomarker in neuromodulation applications. Two critical challenges of microscale neural interfaces are 1) how to apply them to small peripheral nerves, and 2) how to minimize chronic reactivity. A flexible microneedle nerve array (MINA) is developed, which is the first high-density penetrating electrode array made with axon-sized silicon microneedles embedded in low-modulus thin silicone. The design, fabrication, acute recording, and chronic reactivity to an implanted MINA, are presented. Distinctive units are identified in the rat peroneal nerve. The authors also demonstrate a long-term, cuff-free, and suture-free fixation manner using rose bengal as a light-activated adhesive for two time-points. The tissue response is investigated at 1-week and 6-week time-points, including two sham groups and two MINA-implanted groups. These conditions are quantified in the left vagus nerve of rats using histomorphometry. Micro computed tomography (micro-CT) is added to visualize and quantify tissue encapsulation around the implant. MINA demonstrates a reduction in encapsulation thickness over previously quantified interfascicular methods. Future challenges include techniques for precise insertion of the microneedle electrodes and demonstrating long-term recording.",

author = "Dongxiao Yan and Jiman, {Ahmad A.} and Bottorff, {Elizabeth C.} and Patel, {Paras R.} and Dilara Meli and Welle, {Elissa J.} and Ratze, {David C.} and Havton, {Leif A.} and Chestek, {Cynthia A.} and Kemp, {Stephen W.P.} and Bruns, {Tim M.} and Euisik Yoon and Seymour, {John P.}",

note = "Funding Information: The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro-CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro-CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth. Funding Information: The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro‐CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro‐CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1 ). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth. Publisher Copyright: {\textcopyright} 2022 Wiley-VCH GmbH.",

year = "2022",

month = may,

day = "26",

doi = "10.1002/smll.202200311",

language = "English",

volume = "18",

journal = "Small",

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T1 - Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array

AU - Yan, Dongxiao

AU - Jiman, Ahmad A.

AU - Bottorff, Elizabeth C.

AU - Patel, Paras R.

AU - Meli, Dilara

AU - Welle, Elissa J.

AU - Ratze, David C.

AU - Havton, Leif A.

AU - Chestek, Cynthia A.

AU - Kemp, Stephen W.P.

AU - Bruns, Tim M.

AU - Yoon, Euisik

AU - Seymour, John P.

N1 - Funding Information: The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro-CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro-CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth. Funding Information: The authors thank the Stimulating Peripheral Activity to Relieve Conditions (SPARC) management team, Felicia Qashu and Michael Wolfson in particular, for monthly suggestions to advance this work. DRIE etching and design resulted in the controlled needle shape reported here, for which the authors thank Saman Parizi, Shuo Huang, Prof. Mark Kushner, Brian van der Elzen, and the Lurie Nanofabrication Facility staff. The authors thank Hannah Parrish and Zhonghua Ouyang for assistance with nerve sample preparation, and Nancy Senabulya at the Michigan Center for Material Characterization facilities for her technical assistance in micro‐CT imaging. The authors thank Dan Ursu for his advice in the histomorphometry analysis. The authors thank Lauren Zimmerman, Eric Kennedy, Georgios Mentzelopoulos, Hannah Parrish, Nicolos Buitrago, and Nikolas Barrera for their advice and/or assistance with surgical procedures and the Unit for Laboratory Animal Management. The authors thank Maegan Kornexl for her help measuring micro‐CT images. The authors thank Muru Zhou at University of Michigan for her outstanding illustration drawing (Figure 1 ). This research was supported by the National Institutes of Health (NIH) SPARC Program (Award 1OT2OD024907, 1OT2OD026585) and the Texas Institute for Restorative Neurotechnologies at UTHealth. Publisher Copyright: © 2022 Wiley-VCH GmbH.

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N2 - Peripheral nerve mapping tools with higher spatial resolution are needed to advance systems neuroscience, and potentially provide a closed-loop biomarker in neuromodulation applications. Two critical challenges of microscale neural interfaces are 1) how to apply them to small peripheral nerves, and 2) how to minimize chronic reactivity. A flexible microneedle nerve array (MINA) is developed, which is the first high-density penetrating electrode array made with axon-sized silicon microneedles embedded in low-modulus thin silicone. The design, fabrication, acute recording, and chronic reactivity to an implanted MINA, are presented. Distinctive units are identified in the rat peroneal nerve. The authors also demonstrate a long-term, cuff-free, and suture-free fixation manner using rose bengal as a light-activated adhesive for two time-points. The tissue response is investigated at 1-week and 6-week time-points, including two sham groups and two MINA-implanted groups. These conditions are quantified in the left vagus nerve of rats using histomorphometry. Micro computed tomography (micro-CT) is added to visualize and quantify tissue encapsulation around the implant. MINA demonstrates a reduction in encapsulation thickness over previously quantified interfascicular methods. Future challenges include techniques for precise insertion of the microneedle electrodes and demonstrating long-term recording.

AB - Peripheral nerve mapping tools with higher spatial resolution are needed to advance systems neuroscience, and potentially provide a closed-loop biomarker in neuromodulation applications. Two critical challenges of microscale neural interfaces are 1) how to apply them to small peripheral nerves, and 2) how to minimize chronic reactivity. A flexible microneedle nerve array (MINA) is developed, which is the first high-density penetrating electrode array made with axon-sized silicon microneedles embedded in low-modulus thin silicone. The design, fabrication, acute recording, and chronic reactivity to an implanted MINA, are presented. Distinctive units are identified in the rat peroneal nerve. The authors also demonstrate a long-term, cuff-free, and suture-free fixation manner using rose bengal as a light-activated adhesive for two time-points. The tissue response is investigated at 1-week and 6-week time-points, including two sham groups and two MINA-implanted groups. These conditions are quantified in the left vagus nerve of rats using histomorphometry. Micro computed tomography (micro-CT) is added to visualize and quantify tissue encapsulation around the implant. MINA demonstrates a reduction in encapsulation thickness over previously quantified interfascicular methods. Future challenges include techniques for precise insertion of the microneedle electrodes and demonstrating long-term recording.

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Ultraflexible and Stretchable Intrafascicular Peripheral Nerve Recording Device with Axon-Dimension, Cuff-Less Microneedle Electrode Array

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