Pupillometry: Psychology, Physiology, and Function (2024)

Anatomy of the eye

The pupil is a transparent opening in the center of the eye (Figure ​(Figure1).1). Light passes through the surface of the lens that is exposed by the pupil, and is focused onto the retina in the back of the eye. The pupil normally appears black, because the inside of the eye is dark, and not because the pupil is an opaque black surface. (This becomes apparent when a camera flash illuminates the inside of the eye, which under a certain angle makes the pupil appear red.) The diameter of the human pupil varies between roughly 2 and 8 mm; therefore, the pupil can change the amount of light that enters the eye by a factor of roughly 16. The colored area around the pupil is the iris, and it contains the muscles that control pupil size (Figure ​(Figure2).2). The white tissue around the iris is called the sclera. The transparent tissue that covers the iris and the pupil (but not the sclera) is the cornea.

Neural pathways

Pupil size is controlled by two pathways that, although interconnected, are often considered distinct: the parasympathetic constriction pathway and the sympathetic dilation pathway. Different reviews highlight different aspects of these pathways. Below I focus on those areas and connections for which several authoritative reviews agree that they are important for pupil control (see Kardon, 2005; ; ; Szabadi, 2012; ). The information below is adapted from these reviews, and detailed references can be found there, especially in Kardon (2005) and McDougal & Gamlin (2008).

Profile

The pupil light response (PLR), also called the pupil light reflex, is the constriction of the pupil in response to brightness, and the dilation of the pupil in response to darkness. Figure ​Figure44 shows a typical PLR, elicited by 10 s of blue or red light presented on a computer monitor, followed by 20 s of a dark screen.

The profile of a typical PLR looks as follows:

• [Light on] 0–0.2s: This is the latency period during which the pupil does not yet respond. The exact latency depends on many factors, such as stimulus intensity (latencies decrease with stimulus intensity) and age (latencies increase with age) (Ellis, 1981).

• [Light on] 0.2–1.5s: The pupil constricts strongly and rapidly until it reaches its minimum size.

• [Light on] 1.5–10s: The pupil either remains fully constricted while the light remains on, or unconstricts (redilates) slightly. This unconstriction, when it occurs, is sometimes called pupil escape; whether it occurs depends on the color of the light: blue light leads to sustained constriction, whereas red light leads to pupil escape. This difference results from the different photoreceptors that are sensitive to blue and red light, as described below.

• [Light off] 10 s–30s: The pupil gradually recovers to its original size. Dilation due to light offset occurs much more slowly than constriction due to light onset. It can take many seconds for the pupil to fully recover, and recovery is faster for red than blue light, again because of the photoreceptors that are sensitive to red and blue light. After a high-intensity blue light, the pupil remains slightly constricted for many minutes. This is called the post-illumination pupil response (PIPR) ().

Neural basis and photoreceptors

The PLR is driven by all known types of photoreceptors: rods, cones, and intrinsically photosensitive retinal ganglion cells (ipRGCs) (Kardon, 2005; Markwell et al., 2010; ).

Cones are sensitive to color, in the sense that there are three types of cones that are maximally responsive to different colors, and the relative activation of these different cone types allows us to distinguish between different colors. (That is, individual cones do not ‘see color’). Cone density is highest in the fovea, and (compared to rods) cones require intense light to become active; therefore, cones dominate central vision, and vision in medium-to-bright levels of light.

Rods are not sensitive to color, in the sense that all rods are maximally sensitive to the same shade of blueish green, and can therefore not distinguish between different colors. Rods are mostly absent from the fovea, and (compared to cones) respond also to weak light; therefore, rods dominate peripheral vision in darkness.

ipRGCs are ganglion cells that receive input from rods and cones, but also contain a photopigment (melanopsin) themselves (). ipRGCs respond much more slowly to light than rods and cones do. In addition to their role in the PLR (as described below), ipRGCs project to the suprachiasmatic nucleus (SCN) of the hypothalamus (sometimes called the biological clock) to maintain the circadian (day-night) rhythm. ipRGCs respond maximally to blueish light (Markwell et al., 2010). ipRGCs seem to contribute mostly to non-image-forming vision, that is, visual functions that are not accompanied by conscious visual awareness, such as pupil responses and maintenance of circadian rhythm. (That is, we are not consciously aware of the effect that light has on synchronizing our circadian rhythm.) However, some studies suggest that ipRGCs may also play a minor role in conscious visual perception (Ecker et al., 2010; Zaidi et al., 2007).

Rods and cones drive the initial pupil constriction of the PLR (0.2–1.5s). This initial constriction therefore has many of the same properties as regular human vision, including that it is strongest for light presented in central vision (Crawford, 1936; ).

However, input from rods and cones desensitizes quickly; therefore, if the PLR was based only on rod and cone vision, the pupil would rapidly unconstrict even while the light was still on. ipRGCs are the reason why our pupils stay constricted: once rod and cone input reduces, ipRGCs start responding and keep the pupil constricted for as long as the light is on (Gamlin et al., 2007). Figure ​Figure44 shows indirect evidence for the role of ipRGCs in maintaining pupillary constriction: given an equally strong initial constriction, pupil constriction (1.5–10s) is more sustained for blue than red light, because ipRGCs are maximally sensitive to blueish light. ipRGCs also drive the PIPR, which is therefore also strongest for blue light. Simply put: because of rods and cones, the pupil rapidly constricts in response to sudden light increases; but because of ipRGCs, the pupil stays constricted throughout the day (Gooley et al., 2012; Wong, 2012).

Signals from rods, cones, and ipRGCs go to the pretectal olivary nucleus (PON), and from there follow the pupillary constriction pathway as shown in Figure ​Figure3a3a.

Cognitive influences

Historically, the PLR was considered a purely reflexive response to the amount of light that falls on the retina. However, recent studies—and also some recently rediscovered older studies—have shown that the PLR is not merely a reflex, but is affected by how visual input is selected (i.e. visual attention), processed, and interpreted (for reviews, see ; ).

Whereas the PLR is a large response (see Figure ​Figure4),4), cognitive influences on the PLR are generally modest in size. For example, Binda, Pereverzeva, & Murray (2013a) reported that covertly attending (without making an eye movement) to a bright stimulus triggered a pupil constriction that was about three times weaker than that triggered by directly looking at a bright stimulus. In most other studies, cognitive influences on the PLR are not directly contrasted with direct exposure to brightness or darkness; but cognitive influences on the PLR are generally small, corresponding to a pupil-size change of less than 1% () to about 5% ().

Function

How does the PLR help visual perception? This seemingly obvious question does not have a clear-cut answer, and even experts often provide different, though not mutually exclusive, answers (). But several functions are generally assumed to play a role (reviewed in ).

The benefit of a dilated pupil is clear: A large pupil lets a lot of light into the eye, thus increasing the amount of visual information that the brain receives, thus increasing visual sensitivity; therefore, a dilated pupil, compared to a constricted pupil, allows you to better detect faint stimuli. Imagine a cat in the dark, looking for small moving stimuli (mice); this cat would probably benefit from large pupils that capture as much light as possible. The question thus becomes why the pupil is not always maximally dilated: why don’t the eyes always capture as much light as they can?

One answer that may come to mind is that pupil constriction serves to protect the retina from damage due to overexposure. However, there is little evidence that the range of light intensities that we normally encounter can damage the retina, even with a fully dilated pupil (). And when you look directly at the sun (which can damage the retina), retinal light flux is so intense that a constricted pupil offers little protection. But if the PLR does not (primarily) serve to protect the retina from overexposure, then what is it good for?

First, a mobile pupil acts as a buffer when transitioning from brightness to darkness (Barlow, 1972; ). When you are in brightness, rods and cones become light adapted (‘bleached’), which makes them less sensitive to light. When you then go from brightness into darkness, rods and cones need to adapt. Dark adaptation is a gradual process that, especially for rods, takes tens of minutes. During the period that you are in darkness while dark adaptation is not yet complete, vision is impaired. Because the pupil can dilate much more rapidly than rods and cones can adapt, pupil dilation reduces the amount of dark adaptation that is necessary, thus (compared to a static pupil) improving vision during the first few minutes of dark adaptation. (Light adaptation is a very rapid process, and does not appear to benefit as much, or at all, from the PLR).

Second—and related to the pupil near response that will be discussed in the next section—pupil constriction increases depth of field: the range of distances at which vision is sharp (Campbell, 1957; ). This is because a constricted pupil exposes only a small part of the eye’s lens. A small lens, compared to a large lens, suffers less from optical distortions that reduce depth of field. While focusing on a point that is very far away, a fully constricted pupil (±2 mm diameter) provides sharp vision from about 2 m distance to infinity, whereas a fully dilated pupil (±8 mm diameter) provides sharp vision from about 7 m distance to infinity. In most laboratory settings, stimuli are presented on a computer display at a fixed distance, and depth of field is therefore of little importance. However, the real world is three dimensional and contains many relevant objects at many different distances; therefore, in real life, the increased depth of field offered by a constricted pupil may be very important.

Third, pupil constriction increases visual acuity: how well you can discriminate fine detail (; ; Woodhouse, 1975). Analogous to depth of field, this is because a constricted pupil, and thus a small lens, suffers less from optical distortions (spherical and chromatic abberations) that cause optical blur. Woodhouse (1975) estimated that a constricted pupil, compared to a dilated pupil, can improve visual acuity by about 20% in situations in which visual sensitivity is not a limiting factor (i.e. for discrimination of bright, high-contrast gratings). When the pupil becomes too small, a different set of optical distortions (diffractions) emerge that impair, rather than improve, visual acuity; this may be why the minimum size of the human pupil is about 2 mm, just above the size at which these distortions come into play.

The benefits of pupil constriction on visual acuity and depth of field are often described as two separate phenomena, but they are really two sides of the same coin: when the pupil constricts, focus improves for all objects except those that are already in perfect focus. For poorly focused objects, such as objects that are far beyond the point of fixation, the benefit is especially pronounced; this is why pupil constriction leads to a pronounced increase in depth of field. For objects that are fixated and are therefore already in good focus, the benefit is more subtle; therefore, pupil constriction leads to only a subtle increase in visual acuity at fixation. However, focus is never perfect: there are always slight imperfections in the eye’s lens, and different colors have slightly different focal depths, making perfect focus impossible even in theory. Therefore, pupil constriction always improves visual acuity, although the effect can be very small.

The PLR thus likely helps vision by reducing dark adaption, and by optimizing the trade-off between visual acuity and depth of field (which benefit from a small pupil) and visual sensitivity (which benefits from a large pupil, especially in darkness). In humans, these effects seem to be small, and vision would likely not be strongly impaired if the pupil would not respond to light. (Although this is difficult to prove, because there seems to be no naturally occurring condition in which pupil size is fixed while vision is otherwise healthy.) However, other animals have far larger ranges of pupil sizes than humans, and thus may benefit more from the PLR. For example, the area of the slit pupil of the Gecko can change by a factor of 300 (Denton, 1956).

And, even if in some animals (such as humans) the PLR may confer but little advantage, “one should bear in mind that seemingly trivial advantages may become extremely significant in a competitive situation; thus an animal whose pupil can dilate a little more may acquire a distinct competitive edge at dusk, and this could make the difference between starvation and plenty.” (Barlow, 1972, p. 3).

Profile

The pupil near response (PNR), also called the pupil near reflex, is the constriction of the pupil in response to looking at a nearby object, and the dilation of the pupil in response looking at a far-away object. The PNR is certainly the least studied, and perhaps the least understood of all pupil responses. The profile of the PNR, shown in Figure ​Figure5,5, is similar to that of the pupil light response (PLR).

In the example data, again from myself, shown in Figure ​Figure5,5, the PNR is elicited by an auditory cue at 0 s to shift gaze from far (±2 m) to near (±0.1 m), and a second auditory cue at 10 s to shift back from near to far. This shift of gaze was such that, except for vergence eye movements, eye position did not change. The profile of the resulting PNR looks as follows:

• [Far to near] 0–0.6s: This is the latency period of the PNR, relative to the cue onset. This time comprises both the time it takes to process the cue and to shift focus from far to near, and the latency of the PNR proper.

• [Far to near] 0.6s–2s: The pupil constricts strongly until it reaches its minimum size.

• [Far to near] 2s–10s: The pupil remains fully constricted. There is no notable pupil escape in the PNR.

• [Near to far] 10s–12s: The pupil recovers to its original size. This redilation is slower than the constriction; however, it is faster than the redilation after a light response (see Figure ​Figure44).

The near triad

The PNR is part of three eye movements, the near triad, that usually (but not necessarily, e.g. Stakenburg, 1991) occur together (; ). Besides the PNR, the near triad includes: vergence, the inward rotation of the eyes to look at something nearby and the outward rotation of the eyes to look at something far away; and accomodation, the curving of the eye’s lens to focus on a nearby object and the flattening of the lens to focus on a far-away object.

Neural basis

The output pathway of the PNR is the same as that of the PLR, projecting from the Edinger-Westphal nucleus (EWN) to the iris sphincter muscle (see Figure ​Figure3a).3a). However, unlike the PLR, the PNR does not appear to be driven directly by a subcortical pathway, but rather by cortical projections to the EWN (). Which cortical areas are involved in the PNR is not entirely clear; however, there are projections from the frontal eye fields (FEF) and parietal cortex to the EWN that are involved in vergence movements (Gamlin, 2002). Because of the strong association between vergence and the PNR, and the central role of the EWN in pupil constriction, it is possible that these projections also play a role in the PNR.

Cognitive influences

To my knowledge, only two studies have directly investigated cognitive influences on the PNR: one published study by Enright (1987); and one of our own studies that we are currently finalizing (). The results of these studies are interesting yet puzzling, and more research is certainly needed.

Enright (1987) asked participants to look at two-dimensional drawings of three-dimensional boxes (i.e. drawings that conveyed a sense of perspective). Participants viewed these drawings monocularly, with one eye covered. Participants fixated either on the corner of the box that appeared nearby, or on the corner that appeared far away. Even though the drawing was in a single plane, participants nevertheless made vergence movements as if they looked at the nearby or far-away corner of a real three-dimensional box. But there were no corresponding pupil-size changes: the pupil was not smaller when participants looked at the nearby corner, indicating that vergence was not accompanied by a PNR.

However, the results were very different when participants viewed so-called Neckercubes. A Neckercube is an ambiguous box-like drawing, in which the same corner can be perceived as either nearby or far away. Participants looked at this corner, and indicated whether they subjectively perceived it as the nearby or far-away corner. The results for vergence movements were more-or-less the same as for the regular box drawings (although slightly weaker), but vergence was now accompanied by exceptionally large pupil responses: the pupil was smaller when the corner was subjectively nearby as compared to when it was subjectively far away. However, while the direction of the effect was consistent with a PNR, the size of the effect was unrealistically large, casting doubt on whether it truly was a PNR, or rather an artifact of some unrecognized confound.

In one of our own experiments (), we used a setup consisting of three separate displays: a central fixation display at an intermediate distance, a display on the left that was nearby, and a display on the right that was far away (or vice versa). Participants either covertly attended to the nearby or far-away display (while keeping gaze on the central display), or, in a different condition, made an eye movement to the nearby or far-away display. In the covert-attention condition, we found that pupil size did not change as a function of whether participants covertly attended to the nearby or far-away display; this suggests that, unlike the PLR (e.g. Binda et al., 2013a; Mathôt et al., 2013), the PNR is not modulated by covert shifts of attention. In the eye-movement condition, we found that the pupil responded to the distance of the to-be-looked-at display, and, importantly, did so with an extremely low latency; this is reminiscent of the effect of eye-movement preparation on the PLR (Ebitz et al., 2014; Mathôt et al., 2015b). However, these results should be interpreted with caution, because distance is related to other factors that might also affect pupil size, such as brightness and size (i.e. from a retinal point of view, nearby things are generally brighter and larger than far-away things).

In conclusion, it is unclear whether the PNR is affected by cognitive influences. Results from the, as far as I know, only two studies that have investigated this issue suggest that, if cognitive influences on the PNR exist, they are likely smaller than similar influences on the PLR (Enright, 1987; ).

Function

The main function of the PNR is likely to increase depth of field for near vision. As described in the section on the PLR, you can see sharply across a wider range of distances with a small pupil than you can with a large pupil (Campbell, 1957; ). The reason that a large depth of field is especially useful for near vision, is that depth of field is much smaller for nearby than far-away objects; that is, you can simultaneously and sharply see two objects at ten and eleven meters distance, but you cannot simultaneously and sharply see two objects at half and one-and-a-half meters distance.

Profile

“Man may either blush or turn pale when emotionally agitated, but his pupils always dilate.” (Loewenfeld, 1958, p. 237)

The pupil dilates after an arousing stimulus, thought, or emotion. Here I call this the psychosensory pupil response (PPR), because this term aptly indicates that this response is driven by both sensory and psychological stimuli. But the same response is sometimes also referred to as reflex dilation, arousal-related dilation, or effort-related dilation. The profile of the PPR varies depending on how it is elicited, but the example data, again from myself, in Figure ​Figure66 shows a typical PPR elicited by a sound (a brief burst of auditory noise). Figure ​Figure77 shows a typical PPR during a working-memory task ().

Types of psychosensory pupil responses

After decades of intensive study on the PPR, Loewenfeld’s quote from 1958 is still a fair summary of the state of the art: Anything that somehow activates the mind, or anything that increases the mind’s ‘processing load’ (Beatty, 1982), also causes the pupil to dilate (reviewed in ; Einhäuser, 2017; Goldwater, 1972; ). Attempts to link specific cognitive processes to the PPR (not mediated by processing load) are therefore, in my view, doomed to fail. However, a useful distinction can be made between an orienting response, which is a brief pupil dilation that is elicited rapidly and involuntarily after something has captured attention (as in Figure ​Figure6),6), and slower arousal- or mental-effort-related responses, which are linked to high-level cognition (as in Figure ​Figure77).

The adaptive-gain theory

The adaptive-gain theory, proposed first by Aston-Jones & Cohen (2005), is an influential theory that deals primarily with the role of the locus coeruleus (LC) in regulating behavior. Because LC activity correlates strongly with pupil size (), pupillometry has become a popular tool to test predictions of the adaptive-gain theory (e.g. ; ). In my view, this theory has become one of the more interesting frameworks to think about PPRs.

According to Aston-Jones & Cohen (2005), there are two distinct modes of behavior, which they refer to as exploitation and exploration. Exploitation refers to a behavioral mode in which you are engaged in a single task, such as eating or reading a book; in this mode, you are ‘exploiting’ the rewards that a task has to offer, such as food or the pleasure of reading. Exploitation is associated with intermediate, phasic (bursty) LC activity, and, consequently, an intermediate pupil size. In contrast, exploration refers to a mode in which you are easily distracted and tend to switch from one task to another; in this mode, you are ‘exploring’ different tasks, to find the one that offers the highest reward. Exploration is associated with high, tonic (sustained) LC activity, and, consequently, large pupils. (Low LC activity and small pupils are associated with sleepiness.)

According to the adaptive-gain theory, animals alternate exploitation and exploration to optimize reward. The idea is simple: imagine that you are hungry and open a bag of chips. Initially, while you are still hungry, eating the chips offers a high reward, and you therefore continue to ‘exploit’ this activity. But after some time, you are no longer hungry, and eating chips is no longer rewarding; at this point you switch to exploration, and look for something that offers a higher reward than eating chips. For example, you may start browsing Facebook. It is initially rewarding to see what all your friends have been up to, and you therefore ‘exploit’ Facebook for a while. But once you’ve seen all the new posts (and assuming you don’t suffer from social-media addiction), reward declines, and you again switch to exploration to find a new, more rewarding activity. And so the exploitation-exploration cycle continues.

The adaptive-gain theory has a high face validity: it makes a lot of sense that animals should alternate between exploration and exploitation; in a way it is not even a theory, but rather a description of behavior that animals clearly exhibit. However, the claim that you can track these switches in behavior mode using pupillometry is new and fascinating. In my view, evidence for this claim is still preliminary, but the results of several studies are certainly suggestive.

In an experiment by Jepma & Nieuwenhuis (2011), participants performed the Four Armed Bandit task, a variation of the Iowa Gambling Task. In this task, participants freely select a card from one of four possible decks. Each deck is associated with a particular pay-off, and this pay-off changes gradually over time (rather than instantly, as in the Iowa Gambling Task). This task naturally leads to exploitation-exploration cycles in behavior. Once participants discover that a particular deck has a high pay-off, they will keep selecting cards from this deck: exploitation. However, because pay-offs fluctuate gradually, there comes a point at which the once-profitable deck is no longer profitable, and participants consequently start trying other decks: exploration. The crucial finding by Jepma & Nieuwenhuis (2011) was that pupils were larger during exploration (trying out new decks) than during exploitation (sticking to a profitable deck), as predicted by the adaptive-gain theory. The problem with studies of this kind, however elegant, is that they rely on correlations: behavioral mode (exploitation v exploration) is not manipulated experimentally but inferred from behavior, and switches in behavioral mode are generally correlated with other factors, such as an increase in disappointingly low pay-offs in the study by Jepma & Nieuwenhuis (2011).

Jepma & Nieuwenhuis (2011), and many others, looked at average pupil size over longer periods; that is, they found that exploration is accompanied by a large tonic (or baseline) pupil size. But another series of experiments showed that exploration is also accompanied by reduced phasic pupil responses, that is, a reduced transient pupil dilation in response to stimuli (Gilzenrat et al., 2010). In other words, during exploration the pupil is large but less responsive, a pattern that mirrors neural activity of the LC ().

A fruitful way to think about exploitation and exploration, and their relationship to phasic and tonic pupil responses, is by taking a hierarchical view: all but the most trivial tasks are composed of subtasks that themselves are composed of yet simpler subtasks. Let’s trace the task hierarchy of my current situation, from simple to complex: I’m sitting behind my computer, writing this paragraph. Being focused on the task of writing is exploitation, compared to switching to another program, for example to check my email—which would be exploration. But at a higher level, the task of sitting behind my computer at all is exploitation, compared to leaving my desk to get a cup of coffee, which is brewing as I type this—which would be exploration. And at a yet higher level, the task of being at work is exploitation, compared going home—which would be exploration.

We can apply this hierarchical view also to experiments, such as the AX-Continuous Performance Task, in which participants are instructed to press a key whenever they see the letter sequence ‘AX’ (e.g. ). In this context, exploitation would generally refer to being focused on detecting the AX sequence, whereas exploration would generally refer to being less focused and more prone to distraction. But even when participants are focused on detecting the AX sequence—and are therefore engaged in exploitation at this level of description—they still need to occasionally switch from the micro-task of not pressing a key to the micro-task of pressing a key; in other words, detecting the AX sequence and pressing a key is a form of brief (micro-)exploration, accompanied by a brief (phasic) pupil dilation. In other words, sustained (tonic) and brief (phasic) pupil responses may not be qualitatively different, but rather reflect exploration at different levels and time scales.

In summary, the adaptive-gain theory provides a refined description of what PPRs may reflect. Its distinction between exploitation (small pupils) and exploration (large pupils) is similar to the traditional distinction between calmness (small pupils), and arousal and effort (large pupils). But it is more specific, and theoretically more interesting.

Neural basis

The neural pathway of the PPR corresponds to the dilation pathway shown in Figure ​Figure3b.3b. Fast, orienting-response-like pupil dilation is presumably mediated by activity of the intermediate layers of the superior colliculus (iSC) (; C. Wang et al., 2014), and possibly by phasic activation of the locus coeruleus (LC) (). Slower, arousal- and mental-efforted-related pupil dilation is presumably mediated by, or at least correlated with, activity in the hypothalamus and the LC (; Joshi et al., 2016).

Function

Researchers have displayed a remarkable lack of interest in the question of why the PPR exists (see Chapter 6 from Bombeke, 2017 for an exception): why do pupils dilate in response to such a wide range of stimuli as sounds, mental effort, and arousal? How does this help us to see the world better, if indeed it does? Consequently, unlike the PLR and PNR, the function of the PPR is mostly unknown. Several researchers have even explicitly rejected the idea that the PPR has any function at all, and consider it to be a non-functional side effect of changes in neural activity. For example, Beatty and Lucero-Wagoner (2000, p. 142) state that “these exceedingly tiny pupillary movements are too small to be of visual consequence.”

In my view, such easy dismissal is unsatisfying. Not only can tiny effects confer an evolutionary benefit (recall the above quote by Barlow, 1972), but it is not clear to me that the PPR is necessarily a tiny effect. Of course, in a laboratory, psychologists use weak stimuli, such as the mental calculations and pictures of naked women used by Hess and Polt (, 1964). Such stimuli evoke smallish pupillary dilations, although the 20% diameter change observed by Hess & Polt (1960) is far from negligible. And my own example PPRs shown in Figures ​Figures66 and ​and77 are indeed tiny, because I did not feel like subjecting myself to fear of death or extremely loud noise. But an animal that, confronted with a predator, fears for its life surely shows stronger pupil dilation. To my knowledge, how much pupils dilate under extreme conditions is unclear (and perhaps best left unclear for ethical considerations), and it certainly varies strongly from species to species; for example, whereas the surface of the human pupil can change by a factor of about 16, for gekkos it can change by a factor of about 300 (Denton, 1956).

So how could PPRs help visual perception? Stefan Van der Stigchel and I recently proposed an explanation (). As I described in the sections on the PLR and the PNR, large pupils have both advantages, notably increased visual sensitivity, and disadvantages, notably decreased depth of field and visual acuity. Depending on, among other things, the amount of available light, the advantages outweigh the disadvantages, or the other way around. More specifically, in darkness, you need all the visual sensitivity you can get, and your pupils therefore dilate; but in brightness, visual sensitivity is very high (because light is abundant), and the pupils therefore constrict to increase visual acuity and depth of field.

Presumably, the optimal trade-off between visual sensitivity and visual acuity is not fixed, but depends on the situation. More specifically, if you are calmly focused on a task (exploitation, in the terminology of ), visual acuity may be especially important; for example, reading requires fine discrimination, and thus high visual acuity, as do many other tasks. Therefore, in such situations, the optimal trade-off between sensitivity and acuity may shift toward acuity, causing the pupils to constrict. In contrast, if you are aroused and on the look-out for danger and opportunity (exploration, in the terminology of ), visual sensitivity may be especially important; for example, a subtle movement somewhere may indicate danger, and it needs to be detected as quickly as possible. Therefore, in such situations, the trade-off may shift toward sensitivity, causing the pupils to dilate. In this view, the PPR would not be a distinct kind of pupil response (as I’ve depicted it here); rather, it would be yet another way in which more basic pupil responses (i.e. the PLR and PNR) are modulated by high-level cognition.

Currently, there is little evidence for (or against) a functional role of the PPR as I’ve outlined above (and see ). This lack of evidence partly results from the practical difficulties of experimentally manipulating pupil size; that is, to go beyond correlational studies, pupil size needs to be experimentally manipulated, without simultaneously manipulating many other things. This is difficult, but not impossible; for example, artificial pupils can be used (cf. Woodhouse, 1975), the pupil can be dilated with eye drops, or pupil size can be manipulated by changing ambient brightness or color (using the fact that red light leads to a more dilated pupil than blue light, cf. Figure ​Figure4).4). All of these approaches have downsides, but in combination they could provide strong support for (or against) a causal link between pupil responses and performance on various perceptual tasks.

In summary, the function of the PPR may be to find the optimal trade-off between visual sensitivity and acuity for a given situation. In some situations, sensitivity may be more important than acuity, and the pupil may therefore dilate; those situations are generally characterized by high levels of arousal, thus explaining the link between arousal and pupil dilation. In other situations, acuity may be more important than sensitivity, and the pupil may therefore constrict; those situations are generally characterized by calmness.

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