Arousal level changes constantly and it has a profound influence on performance during everyday activities. Fluctuations in arousal are regulated by the autonomic nervous system, which is mainly controlled by the balanced activity of the parasympathetic and sympathetic systems, commonly indexed by heart rate (HR) and galvanic skin response (GSR), respectively. Although a growing number of studies have used pupil size to indicate the level of arousal, research that directly examines the relationship between pupil size and HR or GSR is limited. The goal of this study was to understand how pupil size is modulated by autonomic arousal. Human participants fixated various emotional face stimuli, of which low-level visual properties were carefully controlled, while their pupil size, HR, GSR, and eye position were recorded simultaneously. We hypothesized that a positive correlation between pupil size and HR or GSR would be observed both before and after face presentation. Trial-by-trial positive correlations between pupil diameter and HR and GSR were found before face presentation, with larger pupil diameter observed on trials with higher HR or GSR. However, task-evoked pupil responses after face presentation only correlated with HR. Overall, these results demonstrated a trial-by-trial relationship between pupil size and HR or GSR, suggesting that pupil size can be used as an index for arousal level involuntarily regulated by the autonomic nervous system.

The orienting reflex is initiated by a salient stimulus and facilitates quick, appropriate action. It involves a rapid shift of the eyes, head, and attention and other physiological responses such as changes in heart rate and transient pupil dilation. The SC is a critical structure in the midbrain that selects incoming stimuli based on saliency and relevance to coordinate orienting behaviors, particularly gaze shifts, but its causal role in pupil dilation remains poorly understood in mammals. Here, we examined the role of the primate SC in the control of pupil dynamics. While requiring monkeys to keep their gaze fixed, we delivered weak electrical microstimulation to the SC, so that saccadic eye movements were not evoked. Pupil size increased transiently after microstimulation of the intermediate SC layers (SCi) and the size of evoked pupil dilation was larger on a dim versus bright background. In contrast, microstimulation of the superficial SC layers did not cause pupil dilation. Thus, the SCi is directly involved not only in shifts of gaze and attention, but also in pupil dilation as part of the orienting reflex, and the function of pupil dilation may be related to increasing visual sensitivity. The shared neural mechanisms suggest that pupil dilation may be associated with covert attention.

The sudden appearance of a novel stimulus in the environment initiates a series of orienting responses that include coordinated shifts of gaze and attention, and also transient changes in pupil size. Although numerous studies have identified a significant effect of stimulus saliency on shifts of gaze and attention, saliency effects on pupil size are less understood. To examine salience-evoked pupil responses, we presented visual, auditory, or audiovisual stimuli while monkeys fixated a central visual spot. Transient pupil dilation was elicited after visual stimulus presentation regardless of target luminance relative to background, and auditory stimuli also evoked similar pupil responses. Importantly, the evoked pupil response was modulated by contrast-based saliency, with faster and larger pupil responses following the presentation of more salient stimuli. The initial transient component of pupil dilation was qualitatively similar to that evoked by weak microstimulation of the midbrain superior colliculus. The pupil responses elicited by audiovisual stimuli were well predicted by a linear summation of each modality response. Together, the results suggest that the transient pupil response, as one component of orienting, is modulated by contrast-based saliency, and the superior colliculus is likely involved in its coordination.