Cardio-audio synchronization drives neural surprise response

Christian Pfeiffer,Marzia De Lucia

doi:10.1038/s41598-017-13861-8

Abstract

Successful prediction of future events depends on the brain’s capacity to extract temporal regularities from sensory inputs. Neuroimaging studies mainly investigated regularity processing for exteroceptive sensory inputs (i.e. from outside the body). Here we investigated whether interoceptive signals (i.e. from inside the body) can mediate auditory regularity processing. Human participants passively listened to sound sequences presented in synchrony or asynchrony to their heartbeat while concomitant electroencephalography was recorded. We hypothesized that the cardio-audio synchronicity would induce a brain expectation of future sounds. Electrical neuroimaging analysis revealed a surprise response at 158–270 ms upon omission of the expected sounds in the synchronous condition only. Control analyses ruled out that this effect was trivially based on expectation from the auditory temporal structure or on differences in heartbeat physiological signals. Implicit neural monitoring of temporal regularities across interoceptive and exteroceptive signals drives prediction of future events in auditory sequences.

Highlights

When exposed to sensory inputs within sequence regularities, the brain generates an expectation that the same rules will apply to future sensory events
These post-hoc results based on Global Field Power (GFP) and Global Map Dissimilarity (GMD) were confirmed by a cluster-permutation test showing for Synchronous vs. Baseline at 153–278 ms and for Synchronous vs. Asynchronous at 148–312 ms following R peak a significant positive cluster in posterior-central scalp regions
The analysis showed no significant correlations of Synchronous vs. Asynchronous difference values between GFP and R peak-to-sound onset (RS) variability (R = 0.10, p = 0.71), GFP and sound onset-to-R peak (SR) variability (R = −0.02, p = 0.93), GMD and RS variability (R = −0.47, p = 0.06), GMD and SR variability (R = −0.21, p = 0.44)

Summary

Introduction

When exposed to sensory inputs within sequence regularities, the brain generates an expectation that the same rules will apply to future sensory events. Recent theories based on predictive coding stress a major contribution of interoceptive signals (from inside the body, i.e. visceral, respiratory, cardiac) to time and body perception[32,33] We tested this hypothesis by manipulating the temporal synchronization between sound sequences and the participant’s heartbeat, using either a fixed (Synchronous condition) or a random (Asynchronous condition) temporal interval. Our paradigm aims at providing the first demonstration of violation detection induced by cardio-audio synchronization in non-isochronous auditory sequences based on individually adjusted heartbeat rhythms

Objectives

Results

Conclusion