Neurophysiological metrics of surprise during locomotor uncertainty

It is thought that the brain relies upon Bayesian inference to integrate sensory input with prior beliefs, updating its environmental model through prediction errors-discrepancies between expected and actual sensory input. This study investigates whether and how pupil diameter and sternocleidomastoid (SCM) muscle activity reflect neurophysiological responses to uncertainty during locomotor adaptation.

Twenty-four healthy young adults walked on a split-belt treadmill with probabilistic perturbations (80 % of right heel strikes) triggered by rapid belt decelerations. Pupil diameter, a proxy for cognitive arousal, and SCM activity, indicative of startle responses, were measured to assess adaptation to environmental uncertainty.

The initial 5 strides of Perturbation trial elicited significant increases in pupil diameter (p < 2.2e-16) and SCM activation (p = 9.444e-06), reflecting surprise/novelty and information gain. Pupil diameter reached maximal values during strides 16:50 and before returning to Baseline equivalent values for Perturbation strides beyond 100. SCM activation showed sustained increases relative to Baseline values for perturbed strides for the entirety of the 15-minute Perturbation trial. Generalized Additive Mixed Models revealed non-linear relationships between perturbations, pupil diameter, and SCM activity, with distinct temporal patterns modulated by perturbation status.

These findings suggest that pupil diameter and SCM activity serve as reliable indicators of surprise and adaptation in dynamic locomotor tasks, highlighting coordinated autonomic and neuromuscular responses to uncertainty. This approach offers insights into the neurocognitive mechanisms of motor learning, with implications for neurorehabilitation and adaptive gait strategies.