Pupil diameter tracked during motor adaptation in humans

Pupil diameter, under constant illumination, is known to reflect individuals’ internal states, such as surprise about observation and environmental uncertainty. Despite the growing use of pupillometry in cognitive learning studies as an additional measure for examining internal states, few studies have used pupillometry in human motor learning studies. Here, we provide the first detailed characterization of pupil diameter changes in a short-term reach adaptation paradigm. We measured pupil changes in 121 human participants while they adapted to abrupt, gradual, or switching force field conditions. Sudden increases in movement error caused by the introduction/reversal of the force field resulted in strong phasic pupil dilation during movement accompanied by a transient increase in tonic premovement baseline pupil diameter in subsequent trials. In contrast, pupil responses were reduced when the force field was gradually introduced, indicating that large, unexpected errors drove the changes in pupil responses. Interestingly, however, error-induced pupil responses gradually became insensitive after experiencing multiple force field reversals. We also found an association between baseline pupil diameter and incidental knowledge of the gradually introduced perturbation. Finally, in all experiments, we found a strong co-occurrence of larger baseline pupil diameter with slower reaction and movement times after each rest break. Collectively, these results suggest that tonic baseline pupil diameter reflects one’s belief about environmental uncertainty, whereas phasic pupil dilation during movement reflects surprise about a sensory outcome (i.e., movement error), and both effects are modulated by novelty. Our results provide a new approach for nonverbally assessing participants’ internal states during motor learning. NEW & NOTEWORTHY Pupil diameter is known as a noninvasive window into individuals' internal states. Despite the growing use of pupillometry in cognitive learning studies, it receives little attention in motor learning studies. Here, we characterized the pupil responses in a short-term reach adaptation paradigm by measuring pupil diameter of human participants while they adapted to abrupt, gradual, or switching force field conditions. Our results demonstrate how surprise and uncertainty reflected in pupil diameter develop during motor adaptation.