Cardiac responses to auditory deviants track variations of hierarchical perceptual processing during sleep

editorial reviewedObjectives: Embodied cognition proposes that visceral inputs play a fundamental role in perceptual processing. The evidence showing that variations in arousal can be tracked by modulations of cardiac responses to violations of hierarchical auditory expectations have come so far from pathological low arousal states (Raimondo et al., 2017). We study this question during sleep by investigating cardiac responses to auditory deviants in a local-global paradigm - a modified version of the classic oddball. Methods: We re-analyzed a dataset of 23 healthy adults who heard the local-global paradigm while having a morning nap (Strauss et al., 2015). We tested cardiac modulations after auditory deviants by comparing the time difference between the R-peak of the heartbeat before and after the onset of auditory deviants according to previous methodology (Raimondo et al., 2017). Results: We found differences in cardiac responses before and after the onset of deviants depending on the hierarchical level of prediction and arousal state (3-way repeated measures ANOVA, triple interaction: F(3,196)=3.92, p=0.010). We replicated previous findings that no cardiac modulations are observed after auditory deviants in wakeful subjects (Student’s t-test for local: t(21)=-0.19, p=0.848, global: t(21)=1.93, p=0.134; corrected for multiple comparisons) (Raimondo et al., 2017). No modulations of cardiac responses were also observed in deep NREM sleep (local: t(5)=0.59, p=0.578, global: t(5)=-1.18, p=0.578; corrected for multiple comparisons). However, an acceleration of the heartbeat was found in light NREM and REM sleep after local deviants (light NREM: t(15)=-3.67, p=0.004, REM: t(8)=-2.51, p=0.036; corrected for multiple comparisons), but not after global deviants (NREM: t(15)=1.26, p=0.735, REM: t(8)=1.26, p=0.488; corrected for multiple comparisons). Conclusions: Cardiac modulations to violations of auditory expectations during sleep are consistent with observations at the cerebral level that show a preservation of low-level hierarchical predictions but an absence of high-level hierarchical expectations in the light NREM sleep and REM sleep stages (Strauss et al., 2015). Our results thus confirm that cardiac modulations can track the variations of hierarchical perceptual processing during sleep. Codes and dataframes for statistical analyses can be accessed here: https://gitlab.uliege.be/Matthieu.Koroma/sleep_localglobal Dr. Mélanie Strauss and Dr. Athena Demertzi are co-last authors