Pupil size tracks perceptual content and surprise

Abstract

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.

Multiple Transient Signals in Human Visual Cortex Associated with an Elementary Decision

“…The conditional probability distributions were one of two Gaussians (i.e., relatively predictable; μ = 2 s, σ = 0.2 s or μ = 6 s, σ = 0.6 s, respectively) or a uniform distribution (i.e., unpredictable; μ = 6 s, truncated at 14 s). The effects of the temporal statistics of target disappearances and reappearances on pupil responses are described in a separate report (Kloosterman et al, 2015a). On different runs, subjects either immediately reported the target disappearances and reappearances by button press (Detection-Button), or they silently counted the target disappearances (Detection-Count).…”

“…Because we used a Gabor patch as the target stimulus, the overall stimulus luminance remained constant during physical target onsets and offsets, so that retinal influences on fluctuations in pupil diameter during the task were minimized (Loewenfeld, 1993; Kloosterman et al, 2015a). Subjects completed a total of 19 runs each of the Detection-Count and Detection-Button conditions, respectively, and six runs of the Illusion condition.…”

“…Even the most elementary of such decisions entail a complex cascade of central events. Those decisions include transient activations of prefrontal association cortex (Frässle et al, 2014; Brascamp et al, 2015), top-down feedback interactions between higher-tier and lower-tier cortical regions (Lamme and Roelfsema, 2000; Nienborg and Cumming, 2009; Zagha et al, 2013; van Kerkoerle et al, 2014; Wimmer et al, 2015), transient release of neuromodulators (Aston-Jones and Cohen, 2005; Parikh et al, 2007; Lin et al, 2015), boosts of arousal state (de Gee et al, 2014; Kloosterman et al, 2015a), and changes in fixational eye movements (Bonneh et al, 2010). …”

Spontaneous Fluctuations and Non-linear Ignitions: Two Dynamic Faces of Cortical Recurrent Loops

“…To circumvent this problem, while indirectly monitoring the cognitive state of participants, Yellin et al (2015) opted to measure spontaneous fluctuations in pupil diameter while subjects were resting with their eyes open. Extensive previous research has documented direct links between pupil diameter and cognitive load (Eldar et al, 2013;Kahneman and Beatty, 1966;Kloosterman et al, 2015), so that examining pupil diameter fluctuations during rest and their relationship to spontaneous activity fluctuations could potentially reveal some indication of the cognitive state of individuals without interfering with their resting state.…”

Pupil Sizes Scale with Attentional Load and Task Experience in a Multiple Object Tracking Task

“…However, for about 120 years, pupil sizes have been found to be additionally and systematically influenced by cognitive processing [3, 4]. For instance, pupil size changes have been studied in decision-making [5–8], attention [4, 9–22], emotions [23, 24], language [25], and memory [26–29]. …”