Decision-makers often arrive at different choices when faced with repeated presentations of the same evidence. Variability of behavior is commonly attributed to noise in the brain’s decision-making machinery. We hypothesized that phasic responses of brainstem arousal systems are a significant source of this variability. We tracked pupil responses (a proxy of phasic arousal) during sensory-motor decisions in humans, across different sensory modalities and task protocols. Large pupil responses generally predicted a reduction in decision bias. Using fMRI, we showed that the pupil-linked bias reduction was (i) accompanied by a modulation of choice-encoding pattern signals in parietal and prefrontal cortex and (ii) predicted by phasic, pupil-linked responses of a number of neuromodulatory brainstem centers involved in the control of cortical arousal state, including the noradrenergic locus coeruleus. We conclude that phasic arousal suppresses decision bias on a trial-by-trial basis, thus accounting for a significant component of the variability of choice behavior.DOI: http://dx.doi.org/10.7554/eLife.23232.001

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Changes in pupil size at constant light levels reflect the activity of neuromodulatory brainstem centers that control global brain state. These endogenously driven pupil dynamics can be synchronized with cognitive acts. For example, the pupil dilates during the spontaneous switches of perception of a constant sensory input in bistable perceptual illusions. It is unknown whether this pupil dilation only indicates the occurrence of perceptual switches, or also their content. Here, we measured pupil diameter in human subjects reporting the subjective disappearance and re-appearance of a physically constant visual target surrounded by a moving pattern ('motion-induced blindness' illusion). We show that the pupil dilates during the perceptual switches in the illusion and a stimulus-evoked 'replay' of that illusion. Critically, the switch-related pupil dilation encodes perceptual content, with larger amplitude for disappearance than re-appearance. This difference in pupil response amplitude enables prediction of the type of report (disappearance vs. re-appearance) on individual switches (receiver-operating characteristic: 61%). The amplitude difference is independent of the relative durations of target-visible and target-invisible intervals and subjects' overt behavioral report of the perceptual switches. Further, we show that pupil dilation during the replay also scales with the level of surprise about the timing of switches, but there is no evidence for an interaction between the effects of surprise and perceptual content on the pupil response. Taken together, our results suggest that pupil-linked brain systems track both the content of, and surprise about, perceptual events.

The extent to which different cognitive processes are "embodied" is widely debated. Previous studies have implicated sensorimotor regions such as lateral intraparietal (LIP) area in perceptual decision making. This has led to the view that perceptual decisions are embodied in the same sensorimotor networks that guide body movements. We use event-related fMRI and effective connectivity analysis to investigate whether the human sensorimotor system implements perceptual decisions. We show that when eye and hand motor preparation is disentangled from perceptual decisions, sensorimotor areas are not involved in accumulating sensory evidence toward a perceptual decision. Instead, inferior frontal cortex increases its effective connectivity with sensory regions representing the evidence, is modulated by the amount of evidence, and shows greater task-positive BOLD responses during the perceptual decision stage. Once eye movement planning can begin, however, an intraparietal sulcus (IPS) area, putative LIP, participates in motor decisions. Moreover, sensory evidence levels modulate decision and motor preparation stages differently in different IPS regions, suggesting functional heterogeneity of the IPS. This suggests that different systems implement perceptual versus motor decisions, using different neural signatures.