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Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei

The brainstem dorsal column nuclei (DCN) are essential to inform the brain of tactile and proprioceptive events experienced by the body. However, little is known about how ascending somatosensory information is represented in the DCN. Our objective was to investigate the usefulness of high-frequency...

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Autores principales: Loutit, Alastair J., Shivdasani, Mohit N., Maddess, Ted, Redmond, Stephen J., Morley, John W., Stuart, Greg J., Birznieks, Ingvars, Vickery, Richard M., Potas, Jason R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6448039/
https://www.ncbi.nlm.nih.gov/pubmed/30983977
http://dx.doi.org/10.3389/fnsys.2019.00011
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author Loutit, Alastair J.
Shivdasani, Mohit N.
Maddess, Ted
Redmond, Stephen J.
Morley, John W.
Stuart, Greg J.
Birznieks, Ingvars
Vickery, Richard M.
Potas, Jason R.
author_facet Loutit, Alastair J.
Shivdasani, Mohit N.
Maddess, Ted
Redmond, Stephen J.
Morley, John W.
Stuart, Greg J.
Birznieks, Ingvars
Vickery, Richard M.
Potas, Jason R.
author_sort Loutit, Alastair J.
collection PubMed
description The brainstem dorsal column nuclei (DCN) are essential to inform the brain of tactile and proprioceptive events experienced by the body. However, little is known about how ascending somatosensory information is represented in the DCN. Our objective was to investigate the usefulness of high-frequency (HF) and low-frequency (LF) DCN signal features (SFs) in predicting the nerve from which signals were evoked. We also aimed to explore the robustness of DCN SFs and map their relative information content across the brainstem surface. DCN surface potentials were recorded from urethane-anesthetized Wistar rats during sural and peroneal nerve electrical stimulation. Five salient SFs were extracted from each recording electrode of a seven-electrode array. We used a machine learning approach to quantify and rank information content contained within DCN surface-potential signals following peripheral nerve activation. Machine-learning of SF and electrode position combinations was quantified to determine a hierarchy of information importance for resolving the peripheral origin of nerve activation. A supervised back-propagation artificial neural network (ANN) could predict the nerve from which a response was evoked with up to 96.8 ± 0.8% accuracy. Guided by feature-learnability, we maintained high prediction accuracy after reducing ANN algorithm inputs from 35 (5 SFs from 7 electrodes) to 6 (4 SFs from one electrode and 2 SFs from a second electrode). When the number of input features were reduced, the best performing input combinations included HF and LF features. Feature-learnability also revealed that signals recorded from the same midline electrode can be accurately classified when evoked from bilateral nerve pairs, suggesting DCN surface activity asymmetry. Here we demonstrate a novel method for mapping the information content of signal patterns across the DCN surface and show that DCN SFs are robust across a population. Finally, we also show that the DCN is functionally asymmetrically organized, which challenges our current understanding of somatotopic symmetry across the midline at sub-cortical levels.
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spelling pubmed-64480392019-04-12 Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei Loutit, Alastair J. Shivdasani, Mohit N. Maddess, Ted Redmond, Stephen J. Morley, John W. Stuart, Greg J. Birznieks, Ingvars Vickery, Richard M. Potas, Jason R. Front Syst Neurosci Neuroscience The brainstem dorsal column nuclei (DCN) are essential to inform the brain of tactile and proprioceptive events experienced by the body. However, little is known about how ascending somatosensory information is represented in the DCN. Our objective was to investigate the usefulness of high-frequency (HF) and low-frequency (LF) DCN signal features (SFs) in predicting the nerve from which signals were evoked. We also aimed to explore the robustness of DCN SFs and map their relative information content across the brainstem surface. DCN surface potentials were recorded from urethane-anesthetized Wistar rats during sural and peroneal nerve electrical stimulation. Five salient SFs were extracted from each recording electrode of a seven-electrode array. We used a machine learning approach to quantify and rank information content contained within DCN surface-potential signals following peripheral nerve activation. Machine-learning of SF and electrode position combinations was quantified to determine a hierarchy of information importance for resolving the peripheral origin of nerve activation. A supervised back-propagation artificial neural network (ANN) could predict the nerve from which a response was evoked with up to 96.8 ± 0.8% accuracy. Guided by feature-learnability, we maintained high prediction accuracy after reducing ANN algorithm inputs from 35 (5 SFs from 7 electrodes) to 6 (4 SFs from one electrode and 2 SFs from a second electrode). When the number of input features were reduced, the best performing input combinations included HF and LF features. Feature-learnability also revealed that signals recorded from the same midline electrode can be accurately classified when evoked from bilateral nerve pairs, suggesting DCN surface activity asymmetry. Here we demonstrate a novel method for mapping the information content of signal patterns across the DCN surface and show that DCN SFs are robust across a population. Finally, we also show that the DCN is functionally asymmetrically organized, which challenges our current understanding of somatotopic symmetry across the midline at sub-cortical levels. Frontiers Media S.A. 2019-03-20 /pmc/articles/PMC6448039/ /pubmed/30983977 http://dx.doi.org/10.3389/fnsys.2019.00011 Text en Copyright © 2019 Loutit, Shivdasani, Maddess, Redmond, Morley, Stuart, Birznieks, Vickery and Potas. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Loutit, Alastair J.
Shivdasani, Mohit N.
Maddess, Ted
Redmond, Stephen J.
Morley, John W.
Stuart, Greg J.
Birznieks, Ingvars
Vickery, Richard M.
Potas, Jason R.
Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title_full Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title_fullStr Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title_full_unstemmed Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title_short Peripheral Nerve Activation Evokes Machine-Learnable Signals in the Dorsal Column Nuclei
title_sort peripheral nerve activation evokes machine-learnable signals in the dorsal column nuclei
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6448039/
https://www.ncbi.nlm.nih.gov/pubmed/30983977
http://dx.doi.org/10.3389/fnsys.2019.00011
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