Auditory Salience Detection Across Wake and Sleep States: Mismatch Negativity and Event-Related Spectral Perturbation in the Rat Superior Colliculus.

Abstract

Understanding the detection of salient auditory stimuli by the deep layer of the superior colliculus (dSC) during REM and NREM sleep offers valuable insights into the neurophysiological mechanisms of state-dependent auditory information processing. We recorded local field potentials (LFP) from dSC, electrocorticogram (ECoG) from frontal/parietal cortical regions, and neck electromyogram (EMG) in freely moving rats during sleep and awake states under oddball paradigm auditory stimulations. Our analysis focused on mismatch negativity (MMN) responses and event-related spectral perturbation (ERSP) in slow gamma (30-60 Hz) activity (SGA) and medium gamma (60-95 Hz) activity (MGA) frequency bands in wakefulness, REM and NREM sleep using three different intensities (35-, 55-, 80-dB) of stimulation. Data were analysed using repeated-measure two-way ANOVA and Linear Mixed Model. We found that the dSC exhibited significantly increased MMN responses to salient auditory stimuli across nearly all conditions (p < 0.05), specifically in REM, compared to other vigilance states. Additionally, stimulus intensity in pure tone experiments significantly enhances the MMN peak amplitude (p < 0.0001). The dSC further illustrated state-dependent spectral dynamics: SGA (30-60 Hz) ERSP substantially increased in NREM (p < 0.0001), while MGA (60-95 Hz) ERSP increased in both REM/NREM significantly (p < 0.001). These findings demonstrate that the dSC, a key node within the auditory processing network, retains robust auditory salience detection in sleep states.