Automated sleep classification with chronic neural implants in freely behaving canines

Author:

Mivalt FilipORCID,Sladky Vladimir,Worrell Samuel,Gregg Nicholas M,Balzekas Irena,Kim Inyong,Chang Su-youne,Montonye Daniel R,Duque-Lopez Andrea,Krakorova Martina,Pridalova Tereza,Lepkova Kamila,Brinkmann Benjamin HORCID,Miller Kai J,Van Gompel Jamie J,Denison Timothy,Kaufmann Timothy J,Messina Steven A,St Louis Erik K,Kremen VaclavORCID,Worrell Gregory AORCID

Abstract

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.

Funder

Certicon a.s.

Mayo Clinic

Defense Advanced Research Projects Agency

National Institute of Neurological Disorders and Stroke

České Vysoké Učení Technické v Praze

Medtronic

Publisher

IOP Publishing

Subject

Cellular and Molecular Neuroscience,Biomedical Engineering

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