Pupil-Linked Arousal Determines Variability in Perceptual Decision Making

Decision making between several alternatives is thought to involve the gradual accumulation of evidence in favor of each available choice. This process is profoundly variable even for nominally identical stimuli, yet the neuro-cognitive substrates that determine the magnitude of this variability are poorly understood. Here, we demonstrate that arousal state is a powerful determinant of variability in perceptual decision making. We measured pupil size, a highly sensitive index of arousal, while human subjects performed a motion-discrimination task, and decomposed task behavior into latent decision making parameters using an established computational model of the decision process. In direct contrast to previous theoretical accounts specifying a role for arousal in several discrete aspects of decision making, we found that pupil diameter was uniquely related to a model parameter representing variability in the rate of decision evidence accumulation: Periods of increased pupil size, reflecting heightened arousal, were characterized by greater variability in accumulation rate. Pupil diameter also correlated trial-by-trial with specific patterns of behavior that collectively are diagnostic of changing accumulation rate variability, and explained substantial individual differences in this computational quantity. These findings provide a uniquely clear account of how arousal state impacts decision making, and may point to a relationship between pupil-linked neuromodulation and behavioral variability. They also pave the way for future studies aimed at augmenting the precision with which people make decisions.Author Summary: Variability is a hallmark of how we make decisions between different alternatives: Even when we are presented with identical repetitions of a stimulus, the timing and accuracy of our associated decisions vary dramatically. Representations of variability or ‘noise’ have necessarily been a prominent feature of how cognitive scientists model the decision making process. However, very little is known about the underlying neural processes or psychophysiological states that determine the magnitude of this variability. In this study, we measured people's pupil size as an indicator of their physiological arousal state during performance of a challenging motion-discrimination task, and modelled decisions on this task using an established computational model of the decision process in which evidence gradually accumulates toward a response threshold. We found that arousal state was tightly and uniquely linked to a computational parameter that specifically represents variability in the rate at which people accumulate evidence to inform their decisions: Larger pupil size, both within- and between-individuals, corresponded to greater variability in this critical aspect of decision making. Our findings uncover a potent source of variability in how people make decisions, and forge a new link between the classical construct of arousal and modern theories of decision making.