Figure - available from: Frontiers in Psychology
This content is subject to copyright.
Pupillary responses to a range of screen flicker rates. (A) Observers viewed full monitor screens that flickered at a particular frequency rate (0.3, 0.7, 1.0, 1.7, 2.3, or 3.4 Hz) while their pupil size was recorded with a camera. (B) Examples of pupil size of a selected observer as a function of time in six separate trials with distinct flicker frequencies. The solid and dashed vertical lines indicate the onsets of white and black screens, respectively. (C) Average spectrum of FFT power per flicker frequency across all observers.
Source publication
The muscles that control the pupil are richly innervated by the autonomic nervous system. While there are central pathways that drive pupil dilations in relation to arousal, there is no anatomical evidence that cortical centers involved with visual selective attention innervate the pupil. In this study, we show that such connections must exist. Spe...
Citations
... Under consistent lighting, pupil dilations are tightly correlated with the release of norepinephrine in the brain's locus coeruleus (Rajkowski, 1993;Aston-Jones et al., 1994;Joshi et al., 2016), the neural hub integral to attention. When presented with a periodic visual (Naber et al., 2013) or auditory (Fink et al., 2018) stimulus, the pupil dilates and constricts in tandem with the stimulus presentation, which is thought to be the product of prediction (Schwiedrzik and Sudmann, 2020). Pupillary entrainment can also occur with more complex and naturally varying stimuli such as music (Kang et al., 2014;Kang and Banaji, 2020) or speech (Kang and Wheatley, 2017). ...
The human eye is a rich source of information about where, when, and how we attend. Our gaze paths indicate where and what captures our attention, while changes in pupil size can signal surprise, revealing our expectations. Similarly, the pattern of our blinks suggests levels of alertness and when our attention shifts between external engagement and internal thought. During interactions with others, these cues reveal how we coordinate and share our mental states. To leverage these insights effectively, we need accurate, timely methods to observe these cues as they naturally unfold. Advances in eye-tracking technology now enable real-time observation of these cues, shedding light on mutual cognitive processes that foster shared understanding, collaborative thought, and social connection. This brief review highlights these advances and the new opportunities they present for future research.
... The pupil orienting response occurs within 200-700 ms following the onset of a visual stimulus and manifests as a brief dilation followed by a prominent constriction (Koevoet, Strauch, Van der Stigchel, et al., 2023;Lynn, 2013;Nieuwenhuis et al., 2011;Strauch, Romein, et al., 2022;Strauch, Wang, et al., 2022;Wang & Munoz, 2015). Specifically the pupil orienting constriction is linked to the depth of sensory processing, and thus the intensity of external attention (Barbur & Thomson, 1987;Binda & Murray, 2015;Naber et al., 2013;Strauch, Wang, et al., 2022). Building on this notion, our previous findings demonstrate that stronger orienting constrictions predict the amount and the precision of information committed to VWM (Koevoet, Naber, et al., 2023). ...
Not only is visual attention shifted to objects in the external world, attention can also be directed to objects in memory. We have recently shown that pupil size indexes how strongly items are attended externally, which was reflected in more precise encoding into visual working memory. Using a retro-cuing paradigm, we here replicated this finding by showing that stronger pupil constrictions during encoding were reflective of the depth of encoding. Importantly, we extend this previous work by showing that pupil size also revealed the intensity of internal attention toward content stored in visual working memory. Specifically, pupil dilation during the prioritization of one among multiple internally stored representations predicted the precision of the prioritized item. Furthermore, the dynamics of the pupillary responses revealed that the intensity of internal and external attention independently determined the precision of internalized visual representations. Our results show that both internal and external attention are not all-or-none processes, but should rather be thought of as continuous resources that can be deployed at varying intensities. The employed pupillometric approach allows to unravel the intricate interplay between internal and external attention and their effects on visual working memory.
... Pupil size gradually increased as awareness shifted between the competing stimuli, indicating that pupillary responses could serve as an index of visual awareness. Furthermore, pupillary oscillations have been informative in tracking attention allocation to different locations in the visual field (Naber et al., 2013). ...
... Here, smaller baseline pupil sizes index more precise encoding into VWM. Naber, Alvarez, et al., 2013). In other words, the pupil constricts whenever a bright portion of the visual field is covertly attended, and vice versa, whenever a dark portion of the visual field attended, the pupil dilates. ...
... In other words, the pupil constricts whenever a bright portion of the visual field is covertly attended, and vice versa, whenever a dark portion of the visual field attended, the pupil dilates. This phenomenon allows so-called pupil luminance-tagging (Mathôt & Van der Stigchel, 2015;Naber, Alvarez, et al., 2013), in which distinct stimuli receive distinct luminance levels (i.e., bright and dark). Whenever one of these stimuli is attended, its luminance is more strongly reflected in the pupil responses-this same principle is used in pupil flicker tagging studies (e.g., Naber et al., 2018;Naber, Alvarez, & Nakayama, 2013). ...
... This phenomenon allows so-called pupil luminance-tagging (Mathôt & Van der Stigchel, 2015;Naber, Alvarez, et al., 2013), in which distinct stimuli receive distinct luminance levels (i.e., bright and dark). Whenever one of these stimuli is attended, its luminance is more strongly reflected in the pupil responses-this same principle is used in pupil flicker tagging studies (e.g., Naber et al., 2018;Naber, Alvarez, & Nakayama, 2013). This allows the pupil to reliably track the focus of covert attention (Binda et al., 2014;Mathôt et al., 2013;Mathôt et al., 2016;Mathôt & Van der Stigchel, 2015;Naber, Alvarez, et al., 2013;Strauch, Romein, et al., 2022). ...
Pupillary dynamics reflect effects of distinct and important operations of visual working memory: encoding, maintenance, and prioritization. Here, we review how pupil size predicts memory performance and how it provides novel insights into the mechanisms of each operation. Visual information must first be encoded into working memory with sufficient precision. The depth of this encoding process couples to arousal‐linked baseline pupil size as well as a pupil constriction response before and after stimulus onset, respectively. Subsequently, the encoded information is maintained over time to ensure it is not lost. Pupil dilation reflects the effortful maintenance of information, wherein storing more items is accompanied by larger dilations. Lastly, the most task‐relevant information is prioritized to guide upcoming behavior, which is reflected in yet another dilatory component. Moreover, activated content in memory can be pupillometrically probed directly by tagging visual information with distinct luminance levels. Through this luminance‐tagging mechanism, pupil light responses reveal whether dark or bright items receive more attention during encoding and prioritization. Together, conceptualizing pupil responses as a sum of distinct components over time reveals insights into operations of visual working memory. From this viewpoint, pupillometry is a promising avenue to study the most vital operations through which visual working memory works .
This article is categorized under: Psychology > Attention
Psychology > Memory
Psychology > Theory and Methods
... A pupillometer is a device for measuring the size of a pupil. Beyond medical uses, it is employed in research in various neuroscientific contexts to determine emotional, cognitive or physical states [1], as well as in use in a variety of related applications, such as driving impairment detection for modern cars [2] or human machine interaction [3,4]. An additional application could be remotely deriving EEG-data, since Park and Wang showed a correlation between brain activity and pupillary oscillations [5]. ...
... Spontaneous oscillations, e.g. the well known pupillary unrest in dark conditions, rarely exceed a third of that range, around 300 µm of diameter oscillation amplitudes [7]. Typical experiments performed on the pupillary light response at 1 Hz yield less than 100 µm in oscillation amplitudes [4,8]. State-of-the-art pupillometers are limited to 0.1 % of the pupil diameter in spatial resolution [9], on average = 5 µm, and typical resolutions used in research do not exceed 5 µm either [10]. ...
... Only then we will be able to understand neglect in-depth and to track the efficacy of therapies over time. Here, we present a novel approach that exploits the phenomenon that pupil light responses are modulated by covert attention (Binda et al., 2013;Haab, 1886;Mathôt et al., 2013;Naber et al., 2013) and are able to track the most fundamental attentional deficit in neglect via weakened pupil light responses to stimuli in neglected hemifields. The here presented method shows promise for sensitive and specific longitudinal measurementwith potential for both research and clinical applications. ...
... But how could this help identify deficits in attention instead of more low-level sensory areas? We exploit the phenomenon that pupil light responses are not purely reflexive, but heavily modulated by attention (Binda & Murray, 2015;Naber et al., 2011Naber et al., , 2013Strauch, Wang, et al., 2022): At constant fixation, shifts in covert attention towards dark or bright parts of an object/visual scene result in pupil dilations or constrictions, respectively (Binda et al., 2013;Haab, 1886;Mathôt et al., 2013;Naber et al., 2013;Strauch, Wang, et al., 2022). To elucidate the potential to capture attentional (instead of sensory) deficits, we tested whether subtle, yet systematic attentional biases towards the left side of the visual field described in younger controls ('pseudoneglect') would be revealed by changes in pupil size (Bowers & Heilman, 1980;Jewell & McCourt, 2000;Strauch, Romein, et al., 2022). ...
... But how could this help identify deficits in attention instead of more low-level sensory areas? We exploit the phenomenon that pupil light responses are not purely reflexive, but heavily modulated by attention (Binda & Murray, 2015;Naber et al., 2011Naber et al., , 2013Strauch, Wang, et al., 2022): At constant fixation, shifts in covert attention towards dark or bright parts of an object/visual scene result in pupil dilations or constrictions, respectively (Binda et al., 2013;Haab, 1886;Mathôt et al., 2013;Naber et al., 2013;Strauch, Wang, et al., 2022). To elucidate the potential to capture attentional (instead of sensory) deficits, we tested whether subtle, yet systematic attentional biases towards the left side of the visual field described in younger controls ('pseudoneglect') would be revealed by changes in pupil size (Bowers & Heilman, 1980;Jewell & McCourt, 2000;Strauch, Romein, et al., 2022). ...
Visuospatial neglect is a frequent and disabling disorder, mostly after stroke, that presents in impaired awareness to stimuli on one side of space. Neglect causes disability and functional dependence, even long after the injury. Improving measurements of the core attentional deficit might hold the key for better understanding of the condition and development of treatment. We present a rapid, pupillometry-based method that assesses automatic biases in (covert) attention, without requiring behavioral responses. We exploit the phenomenon that pupil light responses scale with the degree of covert attention to stimuli, and thereby reveal what draws (no) attention. Participants with left-sided neglect after right-sided lesions following stroke (n = 5), participants with hemianopia/quadrantanopia following stroke/trauma (n = 11), and controls (n = 22) were presented with two vertical bars, one of which was white and one of which was black, while fixating the center. We varied which brightness was left and right, respectively across trials. In line with the hypotheses, participants with neglect demonstrated biased pupil light responses to the brightness on the right side. Participants with hemianopia showed similar biases to intact parts of the visual field, whilst controls exhibited no bias. Together, this demonstrates that the pupil light response can reveal not only visual, but also attentional deficits. Strikingly, our pupillometry-based bias estimates were not in agreement with neuropsychological paper-and-pencil assessments conducted on the same day, but were with those administered in an earlier phase post-stroke. Potentially, we pick up on persistent biases in the covert attentional system that participants increasingly compensate for in classical neuropsychological tasks and everyday life. The here proposed method may not only find clinical application, but also advance theory and aid the development of successful restoration therapies by introducing a precise,
longitudinally valid, and objective measurement that might not be affected by compensation.
... The latter is evidenced by findings of a close relationship between the pupillary light reflex and concurrent attention shifts (for reviews, see Laeng & Alnaes, 2019;Mathôt, 2018). For instance, covert shifts of attention towards a bright (or, respectively, dark) stimulus in the periphery consistently evoke a pupillary constriction (or, respectively, dilation), demonstrating that changes in pupil size can be used to track where attention is allocated (Binda et al., 2013;Mathôt et al., 2013Mathôt et al., , 2014Naber et al., 2013). ...
The present study investigated whether the integration of separate parts into a whole-object representation varies with the amount of available attentional resources. To this end, two experiments were performed, which required observers to maintain central fixation while searching in peripheral vision for a target among various distractor configurations. The target could either be a “grouped” whole-object Kanizsa figure, or an “ungrouped” configuration of identical figural parts, but which do not support object completion processes to the same extent. In the experiments, accuracies and changes in pupil size were assessed, with the latter reflecting a marker of the covert allocation of attention in the periphery. Experiment 1 revealed a performance benefit for grouped (relative to ungrouped) targets, which increased with decreasing distance from fixation. By contrast, search for ungrouped targets was comparably poor in accuracy without revealing any eccentricity-dependent variation. Moreover, measures of pupillary dilation mirrored this eccentricity-dependent advantage in localizing grouped targets. Next, in Experiment 2, an additional attention-demanding foveal task was introduced in order to further reduce the availability of attentional resources for the peripheral detection task. This additional task hampered performance overall, alongside with corresponding pupil size changes. However, there was still a substantial benefit for grouped over ungrouped targets in both the behavioral and the pupillometric data. This shows that perceptual grouping scales with the allocation of attention even when only residual attentional resources are available to trigger the representation of a complete (target) object, thus illustrating that object completion operates in the “near absence” of attention.
... Previous studies have shown that the PLR is susceptible to covert attention (Binda et al., 2013;Mathôt et al., 2013;Naber et al., 2013;Unsworth & Robison, 2017). In a study by Mathôt et al. (2013), participants were presented with a display that was vertically divided into a bright and a dark half. ...
... In our study, we investigated the effect of covert attention on the sustained phase of the pupillary light response (PLR), which is mediated by intrinsically photosensitive retinal ganglion cells (ipRGCs); we compared this to the well-established effect of covert attention on the initial PLR (Binda et al., 2013;Mathôt et al., 2013;Naber et al., 2013), which is mediated by rods and . CC-BY 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
In brightness the pupil constricts, while in darkness the pupil dilates; this is known as the pupillary light response (PLR). The PLR is driven by all photoreceptors: rods and cones, which contribute to image-forming vision, as well as intrinsically photosensitive retinal ganglion cells (ipRGCs), which contribute to non-image-forming vision. Rods and cones cause immediate pupil constriction upon light exposure, whereas ipRGCs cause sustained constriction for as long as light exposure continues. Recent studies have shown that the initial PLR is modulated by covert attention; however, it remains unclear whether the same holds for the sustained PLR. Here, we investigated the effect of covert attention on sustained, ipRGC-mediated pupil constriction. We leveraged the fact that ipRGCs are predominantly responsive to blue light, causing the most prominent sustained constriction in response to blue light. Replicating previous studies, we found that the pupil constricted more when either directly looking at, or covertly attending to, bright as compared to dim stimuli (with the same color). We also found that the pupil constricted more when directly looking at blue as compared to red stimuli (with the same luminosity); crucially, however, we did not find any difference in pupil size when covertly attending to blue as compared to red stimuli. This suggests that ipRGC-mediated pupil constriction, and possibly non-image-forming vision more generally, is not modulated by covert attention.
Significance statement
When we think of vision, we generally think of image-forming vision, that is, seeing things. However, vision can also be “non-image-forming”; for example, our day-night rhythm and pupil size are regulated by visual input, but not in a way that gives rise to conscious visual awareness. While visual attention shapes image-forming vision, its influence on non-image forming vision remains unclear. We investigated this by using ipRGCs,which contribute to non-image-forming vision and are responsive to blue light. Aside from replicating the effect of covert attention on image-forming vision, we showed that pupil constriction differed between directly looking at blue/ red stimuli, but not during covert attention to these stimuli. This suggests that non-image forming vision is not influenced by covert visual attention.
... 30 Thus, under complex blur environments, the adaptability of neural adjustment driven by blur characteristics 31 may benefit from task-oriented attention. More importantly, attention involves a wide network of neuronal connections, 32 which could enable the mediation of the oculomotor response regulating retinal environmental blurs, 33 in addition to neural coding of stimuli. However, it remains unknown whether attention can selectively enhance or suppress blur. ...
Purpose:
To investigate the impact of attention orientation in young myopic adults with astigmatism.
Methods:
The effect of attention on foveal meridional performance and anisotropy was measured in corrected myopes with various levels of astigmatism (with-the-rule astigmatism ≤ -0.75D, Axis: 180 ± 20) using orientation-based attention. Attention was manipulated by instructing subjects to attend to either the horizontal or the vertical line of a central pre-stimulus (a pulsed cross) along separate blocks of trials. For each attention condition, meridional acuity and reaction times were measured via an annulus Gabor target situated remotely from the cross and presented at random horizontally and vertically in a two-alternative forced-choice employing two interleaved staircase procedures (one-up/one-down). Attention modulations were estimated by the difference in performance between horizontal and vertical attention.
Results:
Foveal meridional performance and anisotropy were strongly affected by the orientation of attention, which appeared critical for the enhancement of reaction times and resolution. Under congruent orienting of attention, foveal meridional anisotropy was correlated with the amount of defocus for both reaction time and resolution, demonstrating greater vertical performance than horizontal performance as myopia increased. Compatible with an attentional compensation of blur through optimal orienting of attention, vertical attention enhanced reaction times compared to horizontal attention and was accompanied by an increase in overall acuity when myopia increased. Increased astigmatism was associated with smaller attention effects and asymmetry, suggesting potential deficits in the compensation of blur in astigmatic eyes.
Conclusion:
Collectively, attention to orientation plays a significant role in horizontal-vertical foveal meridional anisotropy and can modulate the asymmetry of foveal perception imposed by the optics of the eye in episodes of uncorrected vision. Further work is necessary to understand how attention and refractive errors interact during visual development. These results may have practical implications for methods to enhance vision with attention training in myopic astigmats.
... Above 1 Hz, results might be more accurately quantifiable in a more fine grained time scale. Note, however, that human pupillary oscillations in higher subbands have been linked to luminance effects rather than other cognitive factors (Naber et al., 2013;Peysakhovich et al., 2015). ...
Pupil size covaries with the diffusion rate of the cholinergic and noradrenergic neurons throughout the brain, which are essential to arousal. Recent findings suggest that slow pupil fluctuations during locomotion are an index of sustained activity in cholinergic axons, whereas phasic dilations are related to the activity of noradrenergic axons. Here, we investigated movement induced arousal (i.e., by singing and swaying to music), hypothesising that actively engaging in musical behaviour will provoke stronger emotional engagement in participants and lead to different qualitative patterns of tonic and phasic pupil activity. A challenge in the analysis of pupil data is the turbulent behaviour of pupil diameter due to exogenous ocular activity commonly encountered during motor tasks and the high variability typically found between individuals. To address this, we developed an algorithm that adaptively estimates and removes pupil responses to ocular events, as well as a functional data methodology, derived from Pfaffs' generalised arousal, that provides a new statistical dimension on how pupil data can be interpreted according to putative neuromodulatory signalling. We found that actively engaging in singing enhanced slow cholinergic-related pupil dilations and having the opportunity to move your body while performing amplified the effect of singing on pupil activity. Phasic pupil oscillations during motor execution attenuated in time, which is often interpreted as a measure of sense of agency over movement.
