Filip Mivalt, Vladimir Sladky, Samuel Worrell, Nicholas M Gregg, Irena Balzekas, Inyong Kim, Su-Youne Chang, Daniel R Montonye, Andrea Duque-Lopez, Martina Krakorova, Tereza Pridalova, Kamila Lepkova, Benjamin H Brinkmann, Kai J Miller, Jamie J Van Gompel, Timothy Denison, Timothy J Kaufmann, Steven A Messina, Erik K St Louis, Vaclav Kremen, Gregory A Worrell
{"title":"Automated sleep classification with chronic neural implants in freely behaving canines.","authors":"Filip Mivalt, Vladimir Sladky, Samuel Worrell, Nicholas M Gregg, Irena Balzekas, Inyong Kim, Su-Youne Chang, Daniel R Montonye, Andrea Duque-Lopez, Martina Krakorova, Tereza Pridalova, Kamila Lepkova, Benjamin H Brinkmann, Kai J Miller, Jamie J Van Gompel, Timothy Denison, Timothy J Kaufmann, Steven A Messina, Erik K St Louis, Vaclav Kremen, Gregory A Worrell","doi":"10.1088/1741-2552/aced21","DOIUrl":null,"url":null,"abstract":"<p><p><i>Objective.</i>Long-term intracranial electroencephalography (iEEG) in freely behaving animals provides valuable electrophysiological information and when correlated with animal behavior is useful for investigating brain function.<i>Approach.</i>Here we develop and validate an automated iEEG-based sleep-wake classifier for canines using expert sleep labels derived from simultaneous video, accelerometry, scalp electroencephalography (EEG) and iEEG monitoring. The video, scalp EEG, and accelerometry recordings were manually scored by a board-certified sleep expert into sleep-wake state categories: awake, rapid-eye-movement (REM) sleep, and three non-REM sleep categories (NREM1, 2, 3). The expert labels were used to train, validate, and test a fully automated iEEG sleep-wake classifier in freely behaving canines.<i>Main results</i>. The iEEG-based classifier achieved an overall classification accuracy of 0.878 ± 0.055 and a Cohen's Kappa score of 0.786 ± 0.090. Subsequently, we used the automated iEEG-based classifier to investigate sleep over multiple weeks in freely behaving canines. The results show that the dogs spend a significant amount of the day sleeping, but the characteristics of daytime nap sleep differ from night-time sleep in three key characteristics: during the day, there are fewer NREM sleep cycles (10.81 ± 2.34 cycles per day vs. 22.39 ± 3.88 cycles per night;<i>p</i>< 0.001), shorter NREM cycle durations (13.83 ± 8.50 min per day vs. 15.09 ± 8.55 min per night;<i>p</i>< 0.001), and dogs spend a greater proportion of sleep time in NREM sleep and less time in REM sleep compared to night-time sleep (NREM 0.88 ± 0.09, REM 0.12 ± 0.09 per day vs. NREM 0.80 ± 0.08, REM 0.20 ± 0.08 per night;<i>p</i>< 0.001).<i>Significance.</i>These results support the feasibility and accuracy of automated iEEG sleep-wake classifiers for canine behavior investigations.</p>","PeriodicalId":16753,"journal":{"name":"Journal of neural engineering","volume":"20 4","pages":""},"PeriodicalIF":3.7000,"publicationDate":"2023-08-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10480092/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neural engineering","FirstCategoryId":"5","ListUrlMain":"https://doi.org/10.1088/1741-2552/aced21","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ENGINEERING, BIOMEDICAL","Score":null,"Total":0}
引用次数: 0
Abstract
Objective.Long-term intracranial electroencephalography (iEEG) in freely behaving animals provides valuable electrophysiological information and when correlated with animal behavior is useful for investigating brain function.Approach.Here we develop and validate an automated iEEG-based sleep-wake classifier for canines using expert sleep labels derived from simultaneous video, accelerometry, scalp electroencephalography (EEG) and iEEG monitoring. The video, scalp EEG, and accelerometry recordings were manually scored by a board-certified sleep expert into sleep-wake state categories: awake, rapid-eye-movement (REM) sleep, and three non-REM sleep categories (NREM1, 2, 3). The expert labels were used to train, validate, and test a fully automated iEEG sleep-wake classifier in freely behaving canines.Main results. The iEEG-based classifier achieved an overall classification accuracy of 0.878 ± 0.055 and a Cohen's Kappa score of 0.786 ± 0.090. Subsequently, we used the automated iEEG-based classifier to investigate sleep over multiple weeks in freely behaving canines. The results show that the dogs spend a significant amount of the day sleeping, but the characteristics of daytime nap sleep differ from night-time sleep in three key characteristics: during the day, there are fewer NREM sleep cycles (10.81 ± 2.34 cycles per day vs. 22.39 ± 3.88 cycles per night;p< 0.001), shorter NREM cycle durations (13.83 ± 8.50 min per day vs. 15.09 ± 8.55 min per night;p< 0.001), and dogs spend a greater proportion of sleep time in NREM sleep and less time in REM sleep compared to night-time sleep (NREM 0.88 ± 0.09, REM 0.12 ± 0.09 per day vs. NREM 0.80 ± 0.08, REM 0.20 ± 0.08 per night;p< 0.001).Significance.These results support the feasibility and accuracy of automated iEEG sleep-wake classifiers for canine behavior investigations.
期刊介绍:
The goal of Journal of Neural Engineering (JNE) is to act as a forum for the interdisciplinary field of neural engineering where neuroscientists, neurobiologists and engineers can publish their work in one periodical that bridges the gap between neuroscience and engineering. The journal publishes articles in the field of neural engineering at the molecular, cellular and systems levels.
The scope of the journal encompasses experimental, computational, theoretical, clinical and applied aspects of: Innovative neurotechnology; Brain-machine (computer) interface; Neural interfacing; Bioelectronic medicines; Neuromodulation; Neural prostheses; Neural control; Neuro-rehabilitation; Neurorobotics; Optical neural engineering; Neural circuits: artificial & biological; Neuromorphic engineering; Neural tissue regeneration; Neural signal processing; Theoretical and computational neuroscience; Systems neuroscience; Translational neuroscience; Neuroimaging.