Behavioural and neural signatures of perceptual decision-making are modulated by pupil-linked arousal

Abstract

The timing and accuracy of perceptual decision-making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of various neural processing stages in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of decision-making alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. Reaction times were shorter on trials with lower tonic, and higher phasic arousal. Additionally, these two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of decision-making. Finally, behavioural variability associated with fluctuations in tonic and phasic arousal, indicative of neuromodulators acting on multiple timescales, was mediated by its effects on the EEG markers of attentional engagement, sensory processing and the variability in decision processing.

eLife digest

Driving along a busy street requires you to constantly monitor the behavior of other road users. You need to be able to spot and avoid the car that suddenly changes lane, or the pedestrian who steps out in front of you. How fast you can react to such events depends in part on your brain's level of alertness, or 'arousal'. This in turn depends on chemicals within the brain called neuromodulators.

Neuromodulators are a type of neurotransmitter. But whereas other neurotransmitters enable brain cells to signal to each other, neuromodulators turn the volume of these signals up or down. The activity of brain regions that produce neuromodulators varies over time, leading to changes in brain arousal. These changes take place over different time scales. Sudden unexpected events, such as those on the busy street above, trigger sub-second changes in arousal. But arousal levels also show spontaneous fluctuations over minutes to hours. We can follow these changes in real-time by looking into a participant’s eyes. This is because the brain regions that produce neuromodulators also control pupil size.

Van Kempen et al. have now combined measurements of pupil size with recordings of electrical brain activity. Healthy volunteers learned to press a button as soon as a target appeared on a screen. The larger a volunteer’s pupils were before the target appeared, the more slowly the volunteer responded on that trial. Large baseline pupil size is thought to indicate a high baseline level of brain arousal. By contrast, the larger the increase in pupil size in response to the target, the faster the volunteer responded on that trial. This increase in pupil size is thought to reflect an increase in brain arousal.

The recordings of brain activity provided clues to the underlying mechanisms. In trials with large baseline pupil size – and therefore high baseline arousal – the volunteers’ brains showed more variable responses to the target. But in trials with a large increase in pupil size – and a large increase in arousal – the volunteers’ brains showed less variable responses, as well as stronger signals related to attention.

Neuromodulators thus act on different timescales to influence different aspects of cognitive performance, including attention and target detection. Fluctuating levels of neuromodulator activity may help explain the variability in our behavior. Monitoring pupil size is one way to gain insights into the mechanisms that bring about these changes in neuromodulator activity.