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.

Brain dynamics for confidence-weighted learning

“…Similarly, activation of the locus-coeruleus (and increased pupil size) promotes feature selectivity in the sensory domain (Krishnamurthy et al, 2017;Rodenkirch et al, 2019). Changes in pupil size are also related to changes in the processing of sensory information and performance during perceptual decision making tasks (de Gee et al, 2014(de Gee et al, , 2017, with different effects of phasic and tonic pupil size (van Kempen et al, 2019) as in the present results.…”

Eye pupil signals information gain

“…These tonic pupillary changes have been related to the modes of discharge observed in noradrenergic neurons [29,63,48,47,50,30]. Large phasic responses occur when baseline firing rates of noradrenergic neurons are low and would correspond to small tonic pupil size, whereas large baseline noradrenergic activity would be associated with large tonic pupil size but small phasic responses [71,29,63,72,47]. Indeed, negative correlations between spontaneous changes in tonic and phasic pupil size have been reported repeatedly [29,20,63,44,73,18,74,72], even though task-induced or interindividual changes in tonic and phasic pupil size go often in the same direction [12,21,10,30,25,75].…”

“…The relation between spontaneous changes in tonic pupil size and behaviour follows an inverted u-shape, with optimal performance being associated with intermediate pupil size, evoking Yerkes-Dodson law [63,72,48,47,58]. Large tonic pupil sizes are concurrent with mind-wandering, distractibility and exploratory behaviour [33,30,76,29,77] while very low tonic pupil sizes are associated with low vigilance and sleepiness [78,79,80,63,36,71,72,47].…”

“…The relation between spontaneous changes in tonic pupil size and behaviour follows an inverted u-shape, with optimal performance being associated with intermediate pupil size, evoking Yerkes-Dodson law [63,72,48,47,58]. Large tonic pupil sizes are concurrent with mind-wandering, distractibility and exploratory behaviour [33,30,76,29,77] while very low tonic pupil sizes are associated with low vigilance and sleepiness [78,79,80,63,36,71,72,47]. However, in contrast with aforementioned spontaneous changes, increases in tonic size that are task-induced occur, on the contrary, in conditions of high task demand: when taxing working memory [81], when counting stimuli silently [82], following changes of contingency [25,83,21,10,30,25,26] or in conditions of high uncertainty [12].…”

Predicting lapses of attention with sleep-like slow waves

“…Pupil size was analyzed with custom functions in Matlab and corrected for the occurrence of blinks (see 33 and Supplementary Methods). Pupil size was averaged over the stimulus presentation window for each trial (window length: 0.75 to 1.25s).…”