A human pupil up close. Photo by v2osk via Unsplash.

The world’s largest eyeball belongs to the giant squid. It was measured for the first time in 2012, at roughly a foot across. The pupil alone is almost four inches in diameter, about the size of a big orange. That may not be huge in absolute terms, but, compared to the human eye, it’s gigantic. Our pupils are measured in millimeters, between about 2 and 9, depending on — well, depending on a lot, as we’ll see.

Small as our pupils are — small as even the giant squid’s pupils are — they contain unexpected depths. And over the last fifty years, especially over the last ten, scientists have been plumbing those depths. The pupil, it turns out, offers a vibrant window into the mind. You might even say it seems to have a mind of its own.

We talk about the pupil as if it’s a thing, a structure. Across languages, people describe the pupil with metaphors that suggest solidity [1]. It is commonly seen as a seed or stone. Or even something larger: the phrase “apple of my eye” referred originally to the pupil.

But the pupil is really not like a rock or seed. It’s a void, albeit a small one — a dark chamber in the middle of the iris that admits light through to the retina. It is a lively void, widening and narrowing to adjust the amount of light it lets in. These movements are controlled by two muscles: a dilator that opens the pupil and a sphincter that constricts it.

We may think of the pupil as a solid circular structure, but it is more accurately a hole—a fact captured in this urn figure from the Oaxaca region of Mexico (c. 200–500 CE). Image via Cleveland Museum of Art.

These voids vary spectacularly across the animal kingdom. Not only in size, from the giant squid on down, but also in shape. Ours are, of course, circular. Others are more elliptical, often oriented vertically in predator species and horizontally in prey species. Some, like those of the gecko, are thin slits that resemble a string of pearls; others are W-shaped, rectangular, crescent-like, fan-shaped, even rhomboidal.

Across species, pupils come in myriad different shapes. Vertically oriented pupils, for instance, are associated with ambush predators. Photo by Samuel Scrimshaw via Unsplash.

There’s also wide diversity in how pupils behave. The primary function of the pupil is to regulate light: to admit more when it’s dark and less when it’s bright. Human pupils take about 200 milliseconds to respond to a sudden flash of light, and they don’t reach maximum constriction for about 800 milliseconds. Avian pupils are far faster. Shown the same flash, an owl’s pupil will reach maximum constriction before yours have moved a millimeter.

Avian pupils constrict and dilate much faster than human pupils do—at what seems like lightning speed. Researchers think birds are able to control their pupil changes voluntarily. Photo by Harm Weustink via Wikipedia.

Scientists have noted this “pupillary light response” for at least a millennium. The earliest observations are credited to the Iranian physician and philosopher, Rhazes, around 900 CE. A few centuries on, Leonardo da Vinci would marvel at the phenomenon. “The pupil of the eye changes to as many different sizes as there are differences in the degrees of brightness,” he wrote. “Nature is here establishing a continual equilibrium.” To observe this equilibrium, he suggested staring into a friend’s eye while moving a candle up to their face.

There’s a curious thing about this pupillary light reflex, though: it’s not just triggered by actual light. Show people a photograph with the sun in it, and their pupils will contract. Subtler suggestions of light work, too. Instruct people to imagine bright or dark things, or just make them read words like ‘day’ or ‘night’ and their pupils will respond accordingly.

And things get even curiouser: the pupils also adjust when there’s no light involved at all, not even suggested. It took some time for researchers to make any sense of these “light-independent” pupillary actions. For a long time, they were dubbed “paradoxical.”

A miniature by the artist Hossein Behzad, showing the celebrated Persian polymath Rhazes (865–925 CE) examining a young patient. Rhazes was one of the first to closely observe how the human pupil responds to light—the so-called “pupillary light response”. Image via Wellcome Collection.

The first person to really stare down this paradox was Eckhard Hess, a psychologist and ethologist at the University of Chicago. The story goes that he got interested in pupils after a comment his wife made. He was sitting next to her one evening, flipping through a book of animal photography, when she noted that his pupils were unusually large. He was puzzled. The room was well-lit, so why would this be? The next morning he put together a stack of photos and presented them one by one to his assistant, a young man named James Polt. They were mostly landscape photos, but Hess slipped in an image he thought Polt might find a bit more engaging. As expected, Polt’s pupils visibly dilated to that oddball photo.

The pair published their first findings in a 1960 article in Science magazine titled ‘Pupil Size as Related to Interest Value of Visual Stimuli.’ It was the start of a celebrated research program: Hess and colleagues would go on to present people with photos of pinups and political candidates, babies and plates of food; they had subjects sip lemon juice and listen to music. All while recording their eyes.

The recording part was key. Noticing that pupils change — as Rhazes and Leonardo had centuries earlier — was one thing. Figuring out how to accurately measure those changes was something else.

Closely on the heels of Hess was another young researcher, Daniel Kahneman, then at Harvard University. Kahneman was interested in how the pupils respond to mental demands. In beautiful time series graphs, also published in Science, he and his co-author showed a lockstep relationship between cognitive effort and pupil size. Have a subject try to remember a string of five digits and their pupil would widen by roughly .2 millimeters. Have them try to remember seven digits and it would widen by .5 millimeters.

Later, in his 2011 book, Thinking, Fast and Slow, Kahneman offered an analogy for what was happening in these experiments. “Much like the electricity meter outside your house or apartment, the pupils offer an index of the current rate at which mental energy is used.” It offers a real-time readout, in other words, of how hard we’re thinking [2].

Since Hess and Kahneman’s early contributions, there have been hundreds of further studies on pupil changes. Studies looking at memory, language processing, pitch discrimination, cognitive ability, and the uncanny valley, not to mention poetry, music, and film. Pick a topic psychologists are interested in, and it’s a safe bet the pupils can tell us — or have told us — something about it. In trying to explain the enthusiasm around pupil research, Hess once remarked, “it’s almost as though a portion of the brain were in plain sight for the psychologist to peer at.”

So psychologists were first drawn to the pupil because of what they reveal about our private thoughts. But there’s another side to the pupil, a public side: they are also part of our social lives. It’s not just scientists that notice pupil changes — we all do, whether we realize it or not.

The social importance of eyes is reflected in a broad range of cultural traditions. An example is the “eye miniatures” that were popular in the 18th and 19th centuries in Britain. Image via Cleveland Museum of Art.

The first studies on this social side of pupils were conducted by Eckherd Hess. He showed male subjects pairs of photos of the same woman. In one of the photos, the pupils were retouched to look bigger; in the other they were retouched to look smaller. The men invariably favored the woman with larger pupils.

In a related experiment, people were given two drawings of a man with blank eyes: in one he was smiling and in the other he was scowling. When asked to fill in the eyes, people gave the smiling face bigger pupils than the scowling face [3]. More recent work has found that the preference for larger pupils emerges early, in infancy.

But why this preference for large pupils? Where does it come from? One possibility has been suggested by Mariska Kret, assistant professor of Cognitive Psychology at Leiden University. We may like big pupils, she proposes, because they fit with the so-called “baby schema” — a constellation of traits that make babies and animals disarmingly cute. This schema is often exploited by cartoonists, as she points out. Compare Bambi’s big dark eyes to the Big Bad Wolf’s beady pinpricks.

In cartoons, sympathetic animal characters, such as Bambi, are often drawn with large pupils, whereas unsympathetic characters, such as the Big Bad Wolf, are drawn with beady eyes. An image from the trailer to the film ‘Bambi’ (1942) via Wikipedia.

An important aspect of these findings is that people don’t realize they’re keying on the pupils. When the men in Hess’s studies preferred the large-pupiled woman, they couldn’t say why. As Desmond Morris once put it, our pupils seem to be constantly conducting a “secret exchange of signs.”

An especially dramatic illustration of this “secret exchange” occurs in what is known as pupil mimicry (or pupillary contagion). When we see another person’s pupils widen, our own pupils tend to follow suit. Kret and her colleagues have done some of the most thoroughgoing studies of this phenomenon. In one, they had people play a trust game, and they found that subjects were more likely to trust partners with dilating pupils than partners with constricting pupils. They also found that how much your pupils dilate in response to your partner’s pupils — that is, your degree of pupil mimicry — correlates with how much you trust them. In other studies, Kret and colleagues have also shown that infants as young as 6 months exhibit pupil mimicry. And, it turns out, so do chimps.

Other researchers have started to examine how this mimicry unfolds over time, in real social interaction. In a study from just this summer, Sophie Wohltjen and Thalia Wheatley, of Dartmouth College, looked at what they term “pupillary synchrony” — the coupling of our pupil sizes as we interact. They found evidence for a recurring rhythm: pupillary synchrony builds up over a stretch of conversation, culminating in eye-contact; it then drops off as we maintain that eye contact, and bottoms out right as we break gaze. Needless to say, there’s a lot to be unpacked about this pattern. But there’s no question that our pupils play a richer role in our social lives than many of us suspected.

The pupil reflects different aspects of our cognitive state. But on a more literal level, it reflects—in miniature—what is physically in front of us. This likely accounts for the most common metaphor for the pupil across languages: ‘child of the eye.’ Detail from a 1942 self-portrait by Cor van Teeseling. Image via Rijkmuseum.

Stepping back, what might be the point of all these light-independent, putatively “paradoxical” shifts in our eyes? The value of having our pupils wax and wane in response to light is obvious. The value of having them wax and wane in response to interest, arousal, attention, or effort is less clear. Is there some adaptive benefit to having a portion of our mind out there on display?

Most mysterious of all, perhaps, is the phenomenon of pupil mimicry. What could be the function of this subconscious mirroring? One provocative idea put forth by Mariska Kret and colleagues is that pupil mimicry may have evolved as an “ancient bonding mechanism,” one that promotes connection and trust.

But how ancient? And just how widespread is this phenomenon? We know that chimpanzees show it. What about other species? We don’t know yet and, until we do, the evolutionary function of pupil mimicry is going to be hard to suss out.

We do know, however, that other species do exhibit light-independent pupil changes. Take birds, for instance. A 1974 paper in Nature documented a puzzling pattern in a talking parrot named Seraphita. Right before saying one of the twenty some words she knew, her pupils would contract—quite suddenly—down to about half their size. Somewhat mystified, the authors suggested the behavior could be some kind of social display, or a maybe sign of effort, or perhaps just the result of “neural cross talk.” Similar behaviors are well known to parrot owners today and are often described as “eye pinning.” But their significance remains unknown.

An Amazon parrot exhibiting “eye-pinning”—a constriction of the pupils that is not due to light and is sometimes correlated with other outward behaviors, such as vocalization. Image by Matt Edmonds via Wikipedia (CC by 3.0).

Or take another group of animals: the cephalopods. We now know cephalopod pupils enlarge when these animals are aroused or looking at food — much like the subjects in Hess’s pioneering studies. And some researchers suspect that pupil shifts may feature in cephalopod courtship displays. Sadly, there are no reports yet on the pupillary behaviors of that most gargantuan of cephalopods, the giant squid. But I’m betting it’s pupil, too, may have a mind of its own.

Research on pupils is widening — and no doubt it will continue to do so. After all, there are still more species to examine — a lot more. New techniques are being developed, and new questions keep emerging. Scientists have been staring into these little voids for more than half a century now, but, as with any good void, these don’t seem to have a bottom.

Note: This post originally appeared in audio format on the ‘Many Minds’ podcast (@ManyMindsPod). You can listen to the episode here.

— — —


[1] The most common metaphor for the pupil across languages, according to Brown & Witkowski, characterizes the pupil as a ‘small person of the eye.’ Variants include ‘doll,’ ‘orphan,’ or ‘infant ghost.’ In fact, this metaphor accounts for the connection between the two unrelated-seeming senses of the English word “pupil”—both stem from a Latin word for child or orphan.

[2] For a recent overview of research on pupil size as an index to cognitive effort, see here.

[3] One particularly controversial current debate among cognitive psychologists is whether baseline pupil size correlates with fluid intelligence.

[4] Several of Hess’s studies have recently been replicated, with good (but not perfect) success. See here and here.

Our world is brimming with beings—human, animal, and artificial. We explore how they think, sense, feel, and learn. A project of @DivIntelligence & @kensycoop.