Pupillometry in auditory multistability

Abstract

In multistability, a constant stimulus induces alternating perceptual interpretations. For many forms of visual multistability, the transition from one interpretation to another (“perceptual switch”) is accompanied by a dilation of the pupil. Here we ask whether the same holds for auditory multistability, specifically auditory streaming. Two tones were played in alternation, yielding four distinct interpretations: the tones can be perceived as one integrated percept (single sound source), or as segregated with either tone or both tones in the foreground. We found that the pupil dilates significantly around the time a perceptual switch is reported (“multistable condition”). When participants instead responded to actual stimulus changes that closely mimicked the multistable perceptual experience (“replay condition”), the pupil dilated more around such responses than in multistability. This still held when data were corrected for the pupil response to the stimulus change as such. Hence, active responses to an exogeneous stimulus change trigger a stronger or temporally more confined pupil dilation than responses to an endogenous perceptual switch. In another condition, participants randomly pressed the buttons used for reporting multistability. In Study 1, this “random condition” failed to sufficiently mimic the temporal pattern of multistability. By adapting the instructions, in Study 2 we obtained a response pattern more similar to the multistable condition. In this case, the pupil dilated significantly around the random button presses. Albeit numerically smaller, this pupil response was not significantly different from the multistable condition. While there are several possible explanations–related, e.g., to the decision to respond–this underlines the difficulty to isolate a purely perceptual effect in multistability. Our data extend previous findings from visual to auditory multistability. They highlight methodological challenges in interpreting such data and suggest possible approaches to meet them, including a novel stimulus to simulate the experience of perceptual switches in auditory streaming.

Temporal dynamics of auditory bistable perception correlated with fluctuation of baseline pupil size

“…The PD events rate (Figure 4b) as transient pupil changes were higher when perceptual alternation occurred, which is in line with the previous studies (Einhäuser et al, 2008; Grenzebach et al, 2021). As these transient PD and baseline pupil changes related to cognitive shift are thought to reflect the different LC firing patterns or neural pathways, event‐related changes in pupil size may be triggered by stimulus saliency or surprise upon perceptual transition (Kloosterman et al, 2015).…”

“…To compare by the within-subject design, the participants who were not rejected in both Experiments 1 and 2 were examined in the following analysis. Two-way repeated measures ANOVAs on the averaged PD events with the response content and experiment as within-subject factors revealed that the average number of PD events was larger in alternation trials than in notrials (F(1,18) = 5.973, p = .025, 2 p = 0.249, BF 10 = 2.186), consistent with the previous studies (Einhäuser et al, 2008;Grenzebach et al, 2021). The number of PD events was larger in Experiment 1 than in 2 (F(1,18) = 7.77, p = .012, 2 p = 0.302, BF 10 = 17.622), which could be explained by the higher task demand in Experiment 1, as the LC-NE system reflects a broad range of cognitive processes.…”

“…To assess the relationship between perceptual alternations and transient pupil change reported previously (Einhäuser et al, 2008; Grenzebach et al, 2021; Turi et al, 2018), we calculated the rate of PD/PC events (see Methods). Figure 4a shows the occurrence of PD/PC events for each trial across all subjects, over a period of 2 s before the task response in the previous trial to 4 s after it.…”

“…Event‐related transient pupil dilations, as an index of phasic LC activity, have been observed by changes in cognitive state such as attentional shift, effort, and decision making (de Gee et al, 2014; Mathôt, 2020; Suzuki et al, 2018) as well as perceptual alternations (Einhäuser et al, 2008; Grenzebach et al, 2021; Sato et al, 2020; Turi et al, 2018). Nevertheless, another explanation of the transient pupil dilations, instead of their being caused by perceptual alternation, could be that they are caused by decision making and/or motor responses such as button‐press responses (Einhäuser et al, 2010; Grenzebach et al, 2021; Hupé et al, 2009). To avoid the influence of motor responses or its preparation on the pupil responses, we analyzed baseline pupil size obtained before participants pressed a button or before they were asked to respond (Figure 1d).…”

“…In other words, if the changes in the tonic arousal level through the LC-NE system involves intrinsic perceptual alternation, the baseline pupil-like arousal should reflect a dynamic neural network change with an intrinsic perceptual shift in bistable perception. Along this line, the transient pupil dilation response has been observed around the occurrence of perceptual alternation (Einhäuser et al, 2008;Grenzebach et al, 2021;Hupé et al, 2009;Sato et al, 2020). However, whether there is a relationship between the baseline pupil size as a proxy of the tonic arousal state and the perceptual alternation over timescales longer than a single trial is unknown.…”