TY - JOUR
T1 - Automated sleep state classification of wide-field calcium imaging data via multiplex visibility graphs and deep learning
AU - Zhang, Xiaohui
AU - Landsness, Eric C.
AU - Chen, Wei
AU - Miao, Hanyang
AU - Tang, Michelle
AU - Brier, Lindsey M.
AU - Culver, Joseph P.
AU - Lee, Jin Moo
AU - Anastasio, Mark A.
N1 - Publisher Copyright:
© 2021 The Authors
PY - 2022/1/15
Y1 - 2022/1/15
N2 - 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.
AB - 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.
KW - 2D CNN
KW - Automated sleep state classification
KW - Deep learning
KW - Local sleep
KW - Multiplex visibility graph
KW - Wide-field calcium imaging
UR - http://www.scopus.com/inward/record.url?scp=85120488363&partnerID=8YFLogxK
U2 - 10.1016/j.jneumeth.2021.109421
DO - 10.1016/j.jneumeth.2021.109421
M3 - Article
C2 - 34822945
AN - SCOPUS:85120488363
SN - 0165-0270
VL - 366
JO - Journal of Neuroscience Methods
JF - Journal of Neuroscience Methods
M1 - 109421
ER -