You know that feeling you get when you're being stared at? Out of the corner of your eye, even outside your field of vision, you can just tell someone is checking you out, sizing you up, or trying to make eye contact with you. Sometimes it almost feels like ESP, this ability to detect another person stare, because it often comes at the fringes of our awareness.
But far from being ESP, the perception originates from a system in the brain that's devoted just to detecting where others are looking. This "gaze detection" system is especially sensitive to whether someone's looking directly at you (for example, whether someone's staring at you or at the clock just over your shoulder). Studies that record the activity of single brain cells find that particular cells fire when someone is staring right at you, but—amazingly—not when the observer's gaze is averted just a few degrees to the left or right of you (then different cells fire instead).
This specialized machinery in the brain reveals just how important your gaze is when communicating with others. Where you look conveys how you feel and what your intentions are, what you like and what you don't like, and directs attention to meaningful things in the environment. Further, making direct eye contact is the most frequent and perhaps the most powerful non-verbal signal we exchange with others; it's central to intimacy, intimidation, and social influence. Eye contact is so primal that its meaning extends across animal species: Predators stare intently before they pounce. Infants gaze at their parents to capture their attention. And as you probably know, humans and dogs can express many things to each other through eye contact alone.
Think of a time when you were out in public somewhere and you could sense someone was staring at you, without you even having to look in that person's direction. What information was your (peripheral) visual system using that led to this awareness?
The first things we usually notice are the other person's head and body positions. If either is pointed in your direction, especially in an unnatural way, this is a big tip-off. The most obvious case is when someone's body is pointed away from you, but their head is turned toward you. This then alerts you to pay closer attention to their eyes.
But even when head and body positions don't give us much information, studies find that our peripheral vision can still detect another's gaze remarkably well. How do we do this?
One factor goes back to our gaze detection system, which makes us more sensitive to the position of others' eyes than we realize. Another factor can be deduced by asking yourself this: How are human eyes different in their appearance from the eyes of other animals? What's unique about the anatomy of human eyes?
The biggest difference is that when looking at human eyes, it's easy to distinguish the dark center (the pupil and iris) from the rest of the visible eyeball (the sclera, the white part). These are hard to distinguish in other animals because: 1) in many animals, the pupil and iris cover most of the outward appearance of the eye, and 2) the sclera of other animals tends to be darker than the human sclera.
So humans have the greatest amount of visible white sclera. This contrast between the white sclera and the dark center makes it much easier to tell where someone is looking. We use a simple rule: dark in the middle of the eye = eye contact; dark on the right = looking right; dark on the left = looking left.
Assuming the head is stationary, consider how easy it is to follow the gaze of human eyes compared to the eyes of a gorilla, tiger, lemur, wolf, or owl.
Having such an easily detectable gaze would be a liability for many species, especially predatory ones. As a predator, you don't want others to know you're staring at them, so a darker, less visible sclera is ideal.
But human survival has come to depend more on cooperating and coordinating our efforts with other people, so communication skills have become more critical to our survival. Biologists suggest that our larger, whiter sclera evolved because they vastly improve our ability to communicate with others—the same reason our complex language capacities evolved. However, eye gaze can express many things that spoken language can't, or things that would take too long to verbalize, like imminent dangers in the environment.
True, having these eyes can make it harder to hide our emotions or to sneak up on prey, but on the whole, gaze signaling and gaze detection have been huge assets to us. That ESP-like feeling you get when you're being watched is your brain telling you, in a barely perceptible way, that something meaningful is happening.