An automated sleep-state classification algorithm for quantifying sleep timing and sleep-dependent dynamics of electroencephalographic and cerebral metabolic parameters

Abstract

Introduction: Rodent sleep research uses electroencephalography (EEG) and electromyography (EMG) to determine the sleep state of an animal at any given time. EEG and EMG signals, typically sampled at .100 Hz, are segmented arbitrarily into epochs of equal duration (usually 2-10 seconds), and each epoch is scored as wake, slow-wave sleep (SWS), or rapid-eye-movement sleep (REMS), on the basis of visual inspection. Automated state scoring can minimize the burden associated with state and thereby facilitate the use of shorter epoch durations. Methods: We developed a semiautomated state-scoring procedure that uses a combination of principal component analysis and naïve Bayes classification, with the EEG and EMG as inputs. We validated this algorithm against human-scored sleep-state scoring of data from C57BL/6J and BALB/CJ mice. We then applied a general homeostatic model to characterize the state-dependent dynamics of sleep slow-wave activity and cerebral glycolytic flux, measured as lactate concentration. Results: More than 89% of epochs scored as wake or SWS by the human were scored as the same state by the machine, whether scoring in 2-second or 10-second epochs. The majority of epochs scored as REMS by the human were also scored as REMS by the machine. However, of epochs scored as REMS by the human, more than 10% were scored as SWS by the machine and 18 (10-second epochs) to 28% (2-second epochs) were scored as wake. These biases were not strain-specific, as strain differences in sleep-state timing relative to the light/dark cycle, EEG power spectral profiles, and the homeostatic dynamics of both slow waves and lactate were detected equally effectively with the automated method or the manual scoring method. Error associated with mathematical modeling of temporal dynamics of both EEG slow-wave activity and cerebral lactate either did not differ significantly when state scoring was done with automated versus visual scoring, or was reduced with automated state scoring relative to manual classification. Conclusions: Machine scoring is as effective as human scoring in detecting experimental effects in rodent sleep studies. Automated scoring is an efficient alternative to visual inspection in studies of strain differences in sleep and the temporal dynamics of sleep-related physiological parameters.