Whenever I teach eye movements, I am reminded of how exciting they are. I like that eye movements appear mundane, common, and perhaps even uninteresting. They fly under most people’s wow-o-cool-o-radar, giving all the appearance of a nuts-and-bolts system without lofty aspirations. Despite this unpretentious appearance, eye movements are incredibly interesting and also of the utmost importance to our social selves. There is so much more to eye movements than may at first meet our gaze.

I remember first learning the basics of gaze control in graduate school. The system is delightfully logical and beautifully aligned with our vestibular system. But that is a story for another day. Today I want to tell three stories.

Unilateral eye movement

Virtually all eye movements are conjugate, meaning that the eyes both move and that they move in the same direction. Examples of this are:

• when looking to the left, both eyes move left
• when looking down, both eyes move down

and so on. There is only one exception to the all-eye-movements-are-conjugate rule. The exception is vergence, a movement that we make when we want to fixate on a near object. To see this for yourself, fixate on a far object, something across the street or out the window. Then switch your gaze to fixate on your finger held just in front of your face. Your eyes will converge. This means that the left eye moves rightward and the right eye moves leftward, converging at a spot in the center. Wwhen we switch from looking at a near object back to looking at a far object, the muscles responsible for vergence simply relax. Thus the only active eye movement that is not conjugate is vergence.

With this background, take a look at this video of Leslie Smebak, a second year student at the University of Chicago’s Pritzker Medical School:

Let’s enumerate Leslie’s unusual abilities:

1. abducting (moving it outward) one eye while the other stays adducted
2. adducting (moving it inward toward the nose) one eye while the other still stays adducted

Leslie can do both of these movements with either eye. While she is unilaterally moving one eye the other eye stays in the far adducted position, stuck right up against the nose. My interpretation is that after normal vergence (adducting both eyes), a gaze shift to the side (let’s say left) is initiated. Well to change from vergence to looking left, the only movement needed is  left eye abduction. So off goes the left eye. Now from a leftward gaze position, a vergence movement will result in the unilateral adduction of the left eye – because the right eye is already in the correct position for vergence. Essentially the trick is to move directly between vergence and a sideward gaze. Leslie agreed that her strategy was to start from a converged position and look to the side or vice versa. It is noteworthy that achieving such a degree of unilateral eye control took a great deal of dedicated practice on Leslie’s part. As more evidence that maybe (just maybe, tongue in cheek) unilateral eye movements are not the most natural of abilities, doing these eye movements results in a headache.

It is worth mentioning that I know at least two other people who can make one eye move while the other remains adducted. But no one  can intentionally make any other type of unilateral eye movement. This highlights the essentially conjugate nature of all eye movements except horizontal ones.

I want to tell two other eye movement-related stories that showcase how fabulous eye movements are. Both of these stories are about the social functions of eye movements rather than the nuts and bolts of moving eyes.

At another time, I will share a video of a student who appears to be able to make voluntary smooth pursuit movements. These movements, exemplified by tracking a bird as it flies across the sky with eyes only (i.e. while keeping the head steady) are supposed to only occur when a target is followed. However, after watching this student make a voluntary smooth pursuit, another student and I both practiced (a lot) and both us us believe we can do it too. The circumstances under which this is possible are limited. …. But I digress… this is a matter for another post…..

Dog gaze

This is Woodie, my mother’s dog. He is very good at using his gaze to get what he wants. As Kikusui and colleagues point out, dogs have a paedomorphic face. That delightful word means that their face is child-like, highlighting the link between mother-offspring bonds and dog-human bonds.

In a recent article published in Science, Professor Takefumi Kikusui of Azabu University, just outside Tokyo, dramatically demonstrated the social power of gaze. He and his colleagues studied eye contact between dogs and people. They found that long gazes between dogs and their respective people produced spikes in oxytocin in the dogs, and also in the dogs’ person. Dogs and people that shared short gazes did not show any increase in oxytocin. Nor did wolves, who do not attach to people as do dogs. It was gaze length and not petting that predicted oxytocin release. In a second experiment, oxytocin was administered to dogs and then the gazes that the dogs participated in were measured. Female dogs that received oxytocin looked longer at their people than did female dogs that received saline (control). Even more remarkable, this long gaze from the oxytocin-treated dogs resulted in more oxytocin release from the gazed-at-person!! Thus there is a loop that uses direct gaze to signal social affiliation and  to change the brain accordingly. This loop appears to have been appropriated by domesticated dog breeds. But where did this loop start? How did such socially signaled neuro-hormone release evolve? Well, all indications are that the primal loop between oxytocin and gaze occurs between mammalian mothers and their offspring. Mutual gaze and oxytocin release act to cement attachment between a mammalian mother and her offspring.

You may be wondering, “what about dads?” The answer is less clear mostly because there is less information. However, we do know that the roles of oxytocin and its cousin, vasopressin, are different in males and females. Work by Larry Young of Emory University has highlighted many of the differences observed. In brief, my take is that gaze can serve as a social signal in males as well as females but that 1) the underlying hormones may be different; and 2) the social messages conveyed by oxytocin and vasopressin are likely to include aggression as well as attachment.

A confrontational gaze

Those of you who are as crazy in love with cats as I am are probably wondering, “what about cats?” Most cats don’t appear to interpret eye contact as positive and see it more as a sign of a threat. So let me tell you a story. For reasons that I don’t entirely understand and am not proud of, one day I decided to get into a staring contest with Tula. Tula is the wildest of our three cats. She loves/likes me. She totally adores her other mother. She curls up like a little baby in my spouse’s arms and indeed gazes lovingly into her preferred mother’s eyes. [I have not seen other cats do this. I think it is fairly unusual.] Tula does not gaze at me and rarely sits on my lap although she tolerates my petting her (at arm’s length) and of course, feeding her.

One day, Tula looked up at me from across the room and I widened my eyes – producing “four-sided whites” – and looked directly into Tula’s eyes. We held each other’s gaze for 100-200 seconds, a very long time. Then Tula hissed at me and dove into her cat fort. She ran from me the rest of that day and continued to do so every day for the following ten days. Think about this. Nothing “physical” happened. I did not hurt Tula. All I did was look at Tula. In the process, I managed to send a social signal (of I’m not sure what) and Tula received it (as aggression and hostility). This is advanced social cognition. Impressive!

This is Tula in full aggressive display: arched back, piloerected and a very direct gaze.