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

Authors
  • Zhang, Xiaohui1
  • Landsness, Eric C2
  • Chen, Wei2
  • Miao, Hanyang2
  • Tang, Michelle2
  • Brier, Lindsey M3
  • Culver, Joseph P4
  • Lee, Jin-Moo5
  • Anastasio, Mark A6
  • 1 Department of Bioengineering, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA.
  • 2 Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA.
  • 3 Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
  • 4 Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Biomedical Engineering, Washington University School of Engineering, St. Louis, MO 63130, USA; Department of Electrical and Systems Engineering, Washington University School of Engineering, St. Louis, MO 63130, USA; Department of Physics, Washington University School of Arts and Science, St. Louis, MO 63130, USA.
  • 5 Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Radiology, Washington University School of Medicine, St. Louis, MO 63110, USA; Department of Biomedical Engineering, Washington University School of Engineering, St. Louis, MO 63130, USA.
  • 6 Department of Bioengineering, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA. Electronic address: [email protected].
Type
Published Article
Journal
Journal of neuroscience methods
Publication Date
Jan 15, 2022
Volume
366
Pages
109421–109421
Identifiers
DOI: 10.1016/j.jneumeth.2021.109421
PMID: 34822945
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

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. 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. 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. 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. The hybrid MVG-CNN method accurately classifies sleep states from WFCI data and will enable future sleep-focused studies with WFCI. Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.

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