Cardiac afferent activity modulates early neural signature of error detection during skilled performance

Abstract

Behavioral adaptations during performance rely on predicting and evaluating the consequences of our actions through action monitoring. Previous studies revealed that proprioceptive and exteroceptive signals contribute to error-monitoring processes, which are implemented in the posterior medial frontal cortex. Interestingly, errors also trigger changes in autonomic nervous system activity such as pupil dilation or heartbeat deceleration. Yet, the contribution of implicit interoceptive signals of bodily states to error-monitoring during ongoing performance has been overlooked. This study investigated whether cardiovascular interoceptive signals influence the neural correlates of error processing during performance, with an emphasis on the early stages of error processing. We recorded musicians' electroencephalography and electrocardiogram signals during the performance of highly-trained music pieces. Previous event-related potential (ERP) studies revealed that pitch errors during skilled musical performance are preceded by an error detection signal, the pre-error-negativity (preERN), and followed by a later error positivity (PE). In this study, by combining ERP, source localization and multivariate pattern classification analysis, we found that the error-minus-correct ERP waveform had an enhanced amplitude within 40-100 ms following errors in the systolic period of the cardiac cycle. This component could be decoded from single-trials, was dissociated from the preERN and PE, and stemmed from the inferior parietal cortex, which is a region implicated in cardiac autonomic regulation. In addition, the phase of the cardiac cycle influenced behavioral alterations resulting from errors, with a smaller post-error slowing and less perturbed velocity in keystrokes following pitch errors in the systole relative to the diastole phase of the cardiac cycle. Lastly, changes in the heart rate anticipated the upcoming occurrence of errors. This study provides the first evidence of preconscious visceral information modulating neural and behavioral responses related to early error monitoring during skilled performance.