The role of the pupil in visual perception

The pupil plays a crucial role in vision by regulating the amount of light that reaches the retina, consequently influencing visual processing at multiple levels of the visual system. While traditionally viewed as a reflexive response to changes in ambient light, recent research demonstrates that pupil size is closely tied to cognitive processes, including attention, and
subjective perception. This symposium brings together research that explores the multifaceted role of the pupil in visual perception, highlighting its optical and neural contributions and its modulation by cognitive factors. Through a series of talks, the speakers will demonstrate how pupillometry can be leveraged as a tool for understanding diverse phenomena, from shaping retinal and EEG responses to tracking attentional dynamics and quantifying the costs of eye movements. The talks will address the following questions: How do changes in pupil size affect responses at different stages of the visual pathway? How does this in turn influence behavioral performance across visual and cognitive tasks? Can pupil size reveal the effort associated with saccadic eye movements? Lastly, are there functional benefits of pupil size fluctuations,
including those driven by cognitive factors? By integrating findings from pupillometry, eye movements, retinal activity, and EEG measurements, this symposium provides a comprehensive understanding of the role of the pupil in visual perception.

Talks

Spontaneous fluctuations in pupil size shape retinal responses to visual stimuli

Sebastiaan Mathôt^1*, Daria Weiden¹, Olaf Dimigen¹

¹University of Groningen, The Netherlands
*Corresponding author: s.mathot@rug.nl

Visual perception is shaped at the earliest stage by the size of the eye’s pupil, which determines how much light enters  the eye and how well this light is focused. However, the exact role of pupil size in visual perception is still poorly understood. We recorded pupil size and electrical activity from the retina and brain while healthy human participants viewed full-screen flashes. We found that early retinal responses, which peaked ±25 ms after stimulus onset and predicted subsequent activity over the visual cortex, were strongly affected by stimulus intensity. Importantly, pupil size, at least within the range of naturally occurring fluctuations, did not affect the amplitude of these early retinal responses, despite resulting in substantial changes in retinal light exposure. However, the direction of pupil-size change at the moment of stimulus presentation did modulate the amplitude of early retinal responses, which were enhanced during phases of dilation as compared to constriction. Based on these results, we suggest that fast-acting adaptation processes may normalize early retinal responses with respect to changes in retinal light exposure that result from spontaneous changes in pupil size: an initial form of brightness constancy. These results shed new light on and raise important and previously unasked questions about the role of pupil size in visual perception.

Key words: pupil, visual perception, retinal activity

The effect of covert visual attention on pupil size during perceptual fading

Ana Vilotijević¹* & Sebastiaan Mathôt^1
1University of Groningen, The Netherlands
*Corresponding author: a.vilotijevic@rug.nl

Pupil size is modulated by various cognitive factors such as attention, working memory, mental imagery, and subjective perception. Previous studies examining cognitive effects on pupil size mainly focused on inducing or enhancing a subjective experience of brightness or darkness (for example by asking participants to attend to/ memorize a bright or dark stimulus), and then showing that this affects pupil size. Surprisingly, the inverse has never been done; that is, it is
still unknown what happens when a subjective experience of brightness or darkness is eliminated or strongly reduced even though bright or dark stimuli are physically present. Here, we aim to answer this question by using perceptual fading, a phenomenon where a visual stimulus gradually fades from visual awareness despite its continuous presentation. The study contains two blocks: Fading and Non-Fading. In the Fading block, participants were presented with black and white patches with a fuzzy outline that were presented at the same location throughout the block, thus inducing strong perceptual fading. In contrast, in the Non-Fading block, the patches switched sides on each trial, thus preventing perceptual fading. Participants covertly attended to one of the two patches, indicated by a cue, and reported the offset of one of a set of circles that are displayed on top. We hypothesized that pupil size will be modulated by covert visual attention in the Non-Fading block, but that this effect will not (or to a lesser extent) arise in the Fading block. We found that covert visual attention to bright/ dark does modulate pupil size even during perceptual fading (Fading block), but to a lesser extent than when the perceptual experience of brightness/ darkness is preserved (Non-Fading block). This implies that pupil size is always modulated by covert attention, but that the effect decreases as subjective experience of brightness or darkness decreases. In broader terms, this suggests that cognitive modulations of pupil size reflect a mixture of high-level and lower-level visual processing.

Key words: pupil, attention, visual perception

Saccade selection is driven by physiologically measurable costs

Christoph Strauch^1*, Damian Koevoet¹, Sebastiaan Mathôt², Laura Van Zantwijk^1,3, Stefan Van der Stigchel¹, Marnix Naber¹

¹ Utrecht University, Experimental Psychology, Helmholtz Institute, The Netherlands
² University of Groningen, The Netherlands
³ Humboldt University Berlin, Germany
*Corresponding author: c.strauch@uu.nl

Selecting the next saccade target is one of the most frequent human decisions, shaping perception and by extension much of cognition. State-of-the-art models of saccade selection suggest it to be driven by the observer’s goals, selection history, and by the physical salience of stimuli. Recent models suggest that another factor is needed to understand attentional selection: the cost of shifting the eyes. However elegant and powerful as a predictor in models, these costs were hard to establish in the past. I here present our recent works demonstrating that eye movement costs can be measured physiologically using pupil size as a marker of effort. After establishing costs, we assessed saccade preferences across the same saccade targets using a free-choice paradigm. We found participants to consistently preferring affordable over costly directions. Furthermore, pupil-inferred cost predicted preferences also when manipulating saliency of potential saccade targets. Here, both saliency and cost affected saccade selection. Lastly, we found this link to be robust during a visual search task in natural scenes, suggesting a substantial and generalizable influence of cost on saccade selection.

Key words: saccades, pupil, visual perception

The interplay of spontaneous pupil-size fluctuations and EEG activity in near-threshold
detection

Veera Ruuskanen^1*, Nico Böhler², Sebastiaan Mathôt¹

¹ University of Groningen, The Netherlands
² Ghent University, Belgium
*Corresponding author: v.h.s.ruuskanen@rug.nl

Larger pupils are associated with improved performance in visual detection tasks. This is often attributed to changes in level of arousal as indexed by pupil size. However, changes in pupil size also affect the amount and focus of light on the retina, potentially influencing detection independently of arousal. Such optical effects of pupil size on detection are rarely studied and poorly understood. The goal of this project was to gain a better understanding of how pupil size and arousal (as measured with EEG) are related to each other and to performance in a visual detection task. We collected EEG and pupil data while participants performed a task consisting of detecting faint luminance patches briefly flashed in peripheral vision. Stimulus parameters were adjusted with a staircase procedure to fix performance at approximately 65% accuracy. We performed a mediation analysis within a structural equation modeling framework to investigate the direct and indirect effects present in the data. The results show that larger pupils and theta suppression are both linked to better performance and more stimulus-present responses. Pupil size is also positively correlated with power in the alpha and beta bands, with the latter being a stronger relationship. Importantly, while there was also a mediation effect present, whereby theta power partly mediated the relationship between pupil size and accuracy, the pupil effect could not be completely explained by power in EEG. This suggests that pupil size affects detection in a way that is partly distinct from power in the EEG, and potentially, arousal.

Key words: pupil, arousal, EEG, near-threshold detection