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Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning

BACKGROUND: Wide-field calcium imaging (WFCI) allows for monitoring of cortex-wide neural dynamics in mice. When applied to the study of sleep, WFCI data are manually scored into the sleep states of wakefulness, non-REM (NREM) and REM by use of adjunct EEG and EMG recordings. However, this process i...

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Autores principales: Zhang, Xiaohui, Landsness, Eric C., Chen, Wei, Miao, Hanyang, Tang, Michelle, Brier, Lindsey M., Culver, Joseph P., Lee, Jin-Moo, Anastasio, Mark A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006179/
https://www.ncbi.nlm.nih.gov/pubmed/34822945
http://dx.doi.org/10.1016/j.jneumeth.2021.109421
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author Zhang, Xiaohui
Landsness, Eric C.
Chen, Wei
Miao, Hanyang
Tang, Michelle
Brier, Lindsey M.
Culver, Joseph P.
Lee, Jin-Moo
Anastasio, Mark A.
author_facet Zhang, Xiaohui
Landsness, Eric C.
Chen, Wei
Miao, Hanyang
Tang, Michelle
Brier, Lindsey M.
Culver, Joseph P.
Lee, Jin-Moo
Anastasio, Mark A.
author_sort Zhang, Xiaohui
collection PubMed
description BACKGROUND: Wide-field calcium imaging (WFCI) allows for monitoring of cortex-wide neural dynamics in mice. When applied to the study of sleep, WFCI data are manually scored into the sleep states of wakefulness, non-REM (NREM) and REM by use of adjunct EEG and EMG recordings. However, this process is time-consuming and often suffers from low inter- and intra-rater reliability and invasiveness. Therefore, an automated sleep state classification method that operates on WFCI data alone is needed. NEW METHOD: A hybrid, two-step method is proposed. In the first step, spatial-temporal WFCI data is mapped to multiplex visibility graphs (MVGs). Subsequently, a two-dimensional convolutional neural network (2D CNN) is employed on the MVGs to be classified as wakefulness, NREM and REM. RESULTS: Sleep states were classified with an accuracy of 84% and Cohen’s κ of 0.67. The method was also effectively applied on a binary classification of wakefulness/sleep (accuracy=0.82, κ = 0.62) and a four-class wakefulness/sleep/anesthesia/movement classification (accuracy=0.74, κ = 0.66). Gradient-weighted class activation maps revealed that the CNN focused on short- and long-term temporal connections of MVGs in a sleep state-specific manner. Sleep state classification performance when using individual brain regions was highest for the posterior area of the cortex and when cortex-wide activity was considered. COMPARISON WITH EXISTING METHOD: On a 3-hour WFCI recording, the MVG-CNN achieved a κ of 0.65, comparable to a κ of 0.60 corresponding to the human EEG/EMG-based scoring. CONCLUSIONS: The hybrid MVG-CNN method accurately classifies sleep states from WFCI data and will enable future sleep-focused studies with WFCI.
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spelling pubmed-90061792022-04-13 Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning Zhang, Xiaohui Landsness, Eric C. Chen, Wei Miao, Hanyang Tang, Michelle Brier, Lindsey M. Culver, Joseph P. Lee, Jin-Moo Anastasio, Mark A. J Neurosci Methods Article BACKGROUND: Wide-field calcium imaging (WFCI) allows for monitoring of cortex-wide neural dynamics in mice. When applied to the study of sleep, WFCI data are manually scored into the sleep states of wakefulness, non-REM (NREM) and REM by use of adjunct EEG and EMG recordings. However, this process is time-consuming and often suffers from low inter- and intra-rater reliability and invasiveness. Therefore, an automated sleep state classification method that operates on WFCI data alone is needed. NEW METHOD: A hybrid, two-step method is proposed. In the first step, spatial-temporal WFCI data is mapped to multiplex visibility graphs (MVGs). Subsequently, a two-dimensional convolutional neural network (2D CNN) is employed on the MVGs to be classified as wakefulness, NREM and REM. RESULTS: Sleep states were classified with an accuracy of 84% and Cohen’s κ of 0.67. The method was also effectively applied on a binary classification of wakefulness/sleep (accuracy=0.82, κ = 0.62) and a four-class wakefulness/sleep/anesthesia/movement classification (accuracy=0.74, κ = 0.66). Gradient-weighted class activation maps revealed that the CNN focused on short- and long-term temporal connections of MVGs in a sleep state-specific manner. Sleep state classification performance when using individual brain regions was highest for the posterior area of the cortex and when cortex-wide activity was considered. COMPARISON WITH EXISTING METHOD: On a 3-hour WFCI recording, the MVG-CNN achieved a κ of 0.65, comparable to a κ of 0.60 corresponding to the human EEG/EMG-based scoring. CONCLUSIONS: The hybrid MVG-CNN method accurately classifies sleep states from WFCI data and will enable future sleep-focused studies with WFCI. 2022-01-15 2021-11-22 /pmc/articles/PMC9006179/ /pubmed/34822945 http://dx.doi.org/10.1016/j.jneumeth.2021.109421 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) ).
spellingShingle Article
Zhang, Xiaohui
Landsness, Eric C.
Chen, Wei
Miao, Hanyang
Tang, Michelle
Brier, Lindsey M.
Culver, Joseph P.
Lee, Jin-Moo
Anastasio, Mark A.
Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title_full Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title_fullStr Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title_full_unstemmed Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title_short Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
title_sort automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9006179/
https://www.ncbi.nlm.nih.gov/pubmed/34822945
http://dx.doi.org/10.1016/j.jneumeth.2021.109421
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