Unpredictable threat increases early event-related potential amplitudes and cardiac acceleration: A brain-heart coupling study.

Abstract

In the face of unpredictable threat, rapid processing of external events and behavioral mobilization through early psychophysiological responses are crucial for survival. While unpredictable threat generally enhances early processing, it would seem adaptive to particularly increase sensitivity for unexpected events as they may signal danger. To examine this possibility, n = 77 participants performed an auditory oddball paradigm and received unpredictable shocks in threat but not in safe contexts while a stream of frequent (standard) and infrequent (deviant) tones was presented. We assessed event-related potentials (ERP), heart period (HP), and time-lagged within-subject correlations of single-trial EEG and HP (cardio-EEG covariance tracing, CECT) time-locked to the tones. N1 and P2 ERP amplitudes were generally enhanced under threat. The P3 amplitude was enhanced to deviants versus standards and this effect was reduced in the threat condition. Regarding HP, both threat versus safe and unexpected versus expected tones led to stronger cardiac acceleration, suggesting separate effects of threat and stimulus expectancy on HP. Finally, CECTs revealed two correlation clusters, indicating that single-trial EEG magnitudes in the N1/P2 and P3 time-windows predicted subsequent cardiac acceleration. The current results show that an unpredictable threat context enhances N1 and P2 amplitudes and cardiac acceleration to benign auditory stimuli. They further suggest separable cortical correlates of different effects on cardiac activity: an early N1/P2 correlate associated with threat-effects on HP and a later P3 correlate associated with expectedness-effects. Finally, the results indicate that unpredictable threat attenuates rather than enhances the processing of unexpected benign events during the P3 latency.