Both a Gauge and a Filter: Cognitive Modulations of Pupil Size
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Both a Gauge and a Filter: Cognitive Modulations of Pupil Size
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Over 50 years of research have established that cognitive processes influence pupil size. This has led to the widespread use of pupil size as a peripheral measure of cortical processing in psychology and neuroscience. However, the function of cortical control over the pupil remains poorly understood. Why does visual attention change the pupil light reflex? Why do mental effort and surprise cause pupil dilation? Here, we consider these functional questions as we review and synthesize two literatures on cognitive effects on the pupil: how cognition affects pupil light response and how cognition affects pupil size under constant luminance. We propose that cognition may have co-opted control of the pupil in order to filter incoming visual information to optimize it for particular goals. This could complement other cortical mechanisms through which cognition shapes visual perception.
attention; decision-making; exploration; pupil light reflex; pupil light response (PLR); pupil size; visual perception.
The PLR is correlated with stimulus attention and PLR magnitude can be used to probe the dynamics of visuospatial attention.
(A) The PLR distraction task. In this task, PLR-evoking probes are presented in one of three locations relative to a rewarded target: above fixation, away from all possible target locations (“neutral”), on the same side as the rewarded target (“congruent”), or in the opposite hemifield from the rewarded target (“incongruent”). PLR probes were presented both before and at various latencies after target onset. (B) Some example pupil traces [data from Ebitz and Moore (28)] showing the characteristic light-evoked constriction after an evoking probe (purple) compared to sham-probe trials (gray). (C) Left: Response time effects of PLR probes in each location. Congruent probes sped response times, while incongruent ones slowed response time. Neutral probes had little impact on response time. Right: The evoked PLR strongly predicted the extent to which that probe would capture attention, as measured by response time effects of the probes. (D) PLR magnitude (bigger = more constriction) as a function of the timing of the PLR probe. If the probe was presented before the rewarded target (negative stimulus onset asynchrony), there was no difference between congruent and incongruent probes. All PLRs were suppressed to probes presented immediately after the rewarded target. Then, as monkeys began to prepare a saccade to the rewarded target, congruent probes PLRs (blue) were enhanced relative to both incongruent (red) and neutral (gray). Figures modified from Ebitz et al. (14) and Ebitz (29) under a Creative Commons Attribution license and with permission from copyright holders.
The PLR is bidirectionally modulated by cortical stimulation.
(A) The frontal eye fields (green) are a part of prefrontal cortex responsible for directing gaze and attention. Injecting current into the frontal eye fields produces repeated saccades to the same location in space (the “response field,” dotted circle). Stimulating at very low currents (“microstimulation”) directs covert visual attention to the response field without moving the eye. (B) The PLR stimulation task. Rhesus monkeys hold fixation while PLR-evoking light probes are flashed on the screen. On some trials, microstimulation is delivered in order to direct covert visual attention to one of the two possible probe locations. (C) The pupil light response from an example session on trials where the probe was flashed in the stimulated response field (left), our outside of the stimulated field (right). Pale colors = no stimulation control trials. Saturated colors = stimulation was delivered. Inset) Difference between control and stimulation trials across all sessions. * p < 0.05. Figures modified from Ebitz and Moore (28), reproduced under a Creative Commons Attribution license.
A potential role for the PLR in optimizing acuity in natural vision.
(A) Natural scenes have luminance gradients, such that successive saccades can target regions with very different brightness (Image: Ansel Adams, “Acoma Pueblo. [National Historic Landmark, New Mexico],” U.S. National Archives, identifier #519836). (B) Cartoon illustrating how a tradeoff between signal to noise and optical aberrations could produce different optimal pupil sizes for different luminance regions. The effect of optical aberrations on vision (costs, solid blue line) increase as a function of pupil size. A larger pupil also increases the amount of light passing through, which means that the signal to noise ratio (SNR) would also increase as a function of pupil size, producing a decreasing cost for vision as a function of pupil size (solid gray and black lines). Because luminance varies across the scene, different regions would have different intrinsic signal levels, which would interact with pupil size to determine the costs (compare solid gray and black lines). To find the optimal pupil size across these two conditions, we can calculate the total costs due to both SNR and optical aberrations (dotted gray lines), then find the pupil size that minimizes these total costs (asterisks).
Example images from the Pictorialist and Purist photographic traditions.
(A) “The Firefly,” A photograph in the Pictorialist style by George Seeley, 1911. (Source: Getty Museum, identifier: #84.XM.163.1). Note the soft focus and lack of high spatial frequency detail. (B) A photograph in the Purist style by Ansel Adams. “Jackson Lake, with Teton Ridge in the background.” Taken for the National Park Service, circa 1933–1942. Note the increase in fine, high spatial frequency detail. (Source: U.S. National Archives, identifier: #519909).
The effects of aperture size on depth of field. (Top to bottom) The effects of decreasing aperture size on defocus in three dimensions in a modern digital camera. The large aperture increases the sense of depth in the top photographs, but the small aperture increases the high spatial frequency information in the bottom photographs. Note that the range of aperture sizes used here is larger than the physiological range of the pupil (which is only 2–8mm) and these images were corrected for optical aberrations by processing in the camera (Photo credit: Boris Oicherman).
Baseline pupil size under constant luminance predicts changes in attentional priorities.
(A) In the distraction task (Figure 1A), large, salient distractors are presented in conflict with a rewarded target. Monkeys are faster for congruent distractors and slower for incongruent distractors (Figure 1C). Increasing pupil size magnifies these effects: attention is more affected by the distractors when pupil size is large. (B) In the same task, we can also measure the probability that monkeys would make an “errant saccade” to a task-irrelevant distractor, rather than a rewarded target (these trials were excluded from analysis in A). Errant saccade likelihood increases as a function of pupil size at fixation. Panel (A) is modified from Ebitz et al. (14) and is reproduced under a Creative Commons Attribution license. Panel (B) is modified from Ebitz and Platt (77) with permission from Cell Press and Elsevier.
Eye pupil signals information gain.
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