Autonomic responses to proprioceptive and visual errors during single-trial reach adaptation

Abstract

The autonomic nervous system (ANS) plays a crucial role in coordinating brain and bodily responses to cope with unexpected events. Extensive research in cognitive control has demonstrated that error-induced responses in peripheral autonomic measures, such as pupil diameter and heart rate, correlate with the quality of the subsequent behavioral adjustment. Here, we perform ANS measurements during a motor learning task to investigate error-induced ANS responses in implicit motor learning. In a series of experiments, we measured multimodal autonomic signals including pupil diameter, skin conductance, and heart rate while participants made a reaching movement under occasional proprioceptive or visual perturbations of different magnitudes. We characterized the phasic autonomic responses to the induced errors and evaluated their influence on motor learning, which was quantified by comparing the trials immediately before and after the error event (single-trial reach adaptation). Consistent with previous research, the results revealed the sequence of ANS responses induced by unexpected motor errors; the pupil dilation, increased skin-conductance, and heart rate deceleration. These responses also demonstrated a clear dose-dependent increase in responses to errors in both visual and proprioceptive modalities. Furthermore, a latent factor analysis using motor learning and multimodal autonomic response data allowed us to detect a statistical relationship between the latent autonomic states and the motor learning rate, suggesting the suppression of implicit motor adaptation by error-induced sympathetic activity. These results provide novel insights into how ANS-tagged internal states affect implicit motor learning. Significance statementThe autonomic nervous system (ANS) plays a crucial role in coordinating brain and bodily responses when coping with unexpected situations. Although extensively studied in the field of cognitive control, little is known about whether and how ANS is involved in implicit motor learning. Here, by monitoring multimodal ANS signals (pupil, skin conductance, and heart rate) during a motor adaptation task, we show that ANS measures show a size-dependent phasic response to proprioceptively/visually applied motor errors. We further show that the ANS, especially the sympathetic error response, mediates the suppression of error sensitivity in larger errors. These results provide novel insights into how ANS-tagged internal states, potentially relevant for statistical inference, affect implicit motor learning. Supplementary MaterialsOne Supplementary Material file is available.