But work by Isabel Gauthier of Vanderbilt University demonstrates something more complicated. Show pictures of different cars, and the fusiform activates—in automobile aficionados.112 Show pictures of birds, and ditto among bird-watchers. The fusiform isn’t about faces; it’s about recognizing examples of things from categories that are emotionally salient to each individual.
Thus, studying behavior is useful for understanding the nature of the brain—ah, isn’t it interesting that behavior A arises from the coupling of brain regions X and Y. And sometimes studying the brain is useful for understanding the nature of behavior—ah, isn’t it interesting that brain region A is central to both behavior X and behavior Y. For example, to me the most interesting thing about the amygdala is its dual involvement in both aggression and fear; you can’t understand the former without recognizing the relevance of the latter.
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A final point related to the core of this book: While this neurobiology is mighty impressive, the brain is not where a behavior “begins.” It’s merely the final common pathway by which all the factors in the chapters to come converge and create behavior.
Three
Seconds to Minutes Before
Nothing comes from nothing. No brain is an island.
Thanks to messages bouncing around your brain, a command has been sent to your muscles to pull that trigger or touch that arm. Odds are that a short time earlier, something outside your brain prompted this to happen, raising this chapter’s key questions: (a) What outside stimulus, acting through what sensory channel and targeting which parts of the brain, prompted this? (b) Were you aware of that environmental stimulus? (c) What stimuli had your brain made you particularly sensitive to? And, of course, (d) what does this tell us about our best and worst behaviors?
Varied sensory information can prompt the brain into action. This can be appreciated by considering this variety in other species. Often we’re clueless about this because animals can sense things in ranges that we can’t, or with sensory modalities we didn’t know exist. Thus, you must think like the animal to learn what is happening. We’ll begin by seeing how this pertains to the field of ethology, the science of interviewing an animal in its own language.
UNIVERSAL RULES VERSUS KNOBBY KNEES
Ethology formed in Europe in the early twentieth century in response to an American brand of psychology, “behaviorism.” Behaviorism descended from the introduction’s John Watson; the field’s famed champion was B. F. Skinner. Behaviorists cared about universalities of behavior across species. They worshipped a doozy of a seeming universal concerning stimulus and response: rewarding an organism for a behavior makes the organism more likely to repeat that behavior, while failure to get rewarded or, worse, punishment for it, makes the organism less likely to repeat it. Any behavior can be made more or less common through “operant conditioning” (a term Skinner coined), the process of controlling the rewards and punishments in the organism’s environment.
Thus, for behaviorists (or “Skinnerians,” a term Skinner labored to make synonymous) virtually any behavior could be “shaped” into greater or lesser frequency or even “extinguished” entirely.
If all behaving organisms obeyed these universal rules, you might as well study a convenient species. Most behaviorist research was done on rats or, Skinner’s favorite, pigeons. Behaviorists loved data, no-nonsense hard numbers; these were generated by animals pressing or pecking away at levers in “operant conditioning boxes” (aka “Skinner boxes”). And anything discovered applied to any species. A pigeon is a rat is a boy, Skinner preached. Soulless droid.*
Behaviorists were often right about behavior but wrong in really important ways, as many interesting behaviors don’t follow behaviorist rules.*1 Raise an infant rat or monkey with an abusive mother, and it becomes more attached to her. And behaviorist rules have failed when humans love the wrong abusive person.
Meanwhile, ethology was emerging in Europe. In contrast with behaviorism’s obsession with uniformity and universality of behavior, ethologists loved behavioral variety. They’d emphasize how every species evolves unique behaviors in response to unique demands, and how one had to open-mindedly observe animals in their natural habitats to understand them (“Studying rat social behavior in a cage is like studying dolphin swimming behavior in a bathtub” is an ethology adage). They’d ask, What, objectively, is the behavior? What triggered it? Did it have to be learned? How did it evolve? What is the behavior’s adaptive value? Nineteenth-century parsons went into nature to collect butterflies, revel in the variety of wing colors, and marvel at what God had wrought. Twentieth-century ethologists went into nature to collect behavior, revel in its variety, and marvel at what evolution had wrought. In contrast to lab coat–clad behaviorists, ethologists tromped around fields in hiking shoes and had fetching knobby knees.*
Sensory Triggers of Behavior in Some Other Species
Using an ethological framework, we now consider sensory triggers of behavior in animals.*2 First there’s the auditory channel. Animals vocalize to intimidate, proclaim, and seduce. Birds sing, stags roar, howler monkeys howl, orangutans give territorial calls audible for miles. As a subtle example of information being communicated, when female pandas ovulate, their vocalizations get higher, something preferred by males. Remarkably, the same shift and preference happens in humans.
There are also visual triggers of behavior. Dogs crouch to invite play, birds strut their plumage, monkeys display their canines menacingly with “threat yawns.” And there are visual cues of cute baby–ness (big eyes, shortened muzzle, round forehead) that drive mammals crazy, motivating them to care for the kid. Stephen Jay Gould noted that the unsung ethologist Walt Disney understood exactly what alterations transformed rodents into Mickey and Minnie.*3
Then there are animals signaling in ways we can’t detect, requiring creativity to interview an animal in its own language.4 Scads of mammals scent mark with pheromones—odors that carry information about sex, age, reproductive status, health, and genetic makeup. Some snakes see in infrared, electric eels court with electric songs, bats compete by jamming one another’s feeding echolocation signals, and spiders identify intruders by vibration patterns on their webs. How about this: tickle a rat and it chirps ultrasonically as its mesolimbic dopamine system is activated.
Back to the rhinencephalon/limbic system war and the resolution ethologists already knew: for a rodent, emotion is typically triggered by olfaction. Across species the dominant sensory modality—vision, sounds, whichever—has the most direct access to the limbic system.
Under the Radar: Subliminal and Unconscious Cuing
It’s easy to see how the sight of a knife, the sound of a voice calling your name, a touch on your hand can rapidly alter your brain.5 But crucially, tons of subliminal sensory triggers occur—so fleeting or minimal that we don’t consciously note them, or of a type that, even if noted, seems irrelevant to a subsequent behavior.
Subliminal cuing and unconscious priming influence numerous behaviors unrelated to this book. People think potato chips taste better when hearing crunching sounds. We like a neutral stimulus more if, just before seeing it, a picture of a smiling face is flashed for a twentieth of a second. The more expensive a supposed (placebo) painkiller, the more effective people report the placebo to be. Ask subjects their favorite detergent; if they’ve just read a paragraph containing the word “ocean,” they’re more likely to choose Tide—and then explain its cleaning virtues.6
Thus, over the course of seconds sensory cues can shape your behavior unconsciously.
A hugely unsettling sensory cue concerns race.7 Our brains are incredibly attuned to skin color. Flash a face for less than a tenth of a second (one hundred milliseconds), so short a time that people aren’t even sure they’ve seen something. Have them guess the race of the pictured face, and there’s a better-than-even chance of accuracy. We may claim to judge someone by the content of th
eir character rather than by the color of their skin. But our brains sure as hell note the color, real fast.
By one hundred milliseconds, brain function already differs in two depressing ways, depending on the race of the face (as shown with neuroimaging). First, in a widely replicated finding, the amygdala activates. Moreover, the more racist someone is in an implicit test of race bias (stay tuned), the more activation there is.8
Similarly, repeatedly show subjects a picture of a face accompanied by a shock; soon, seeing the face alone activates the amygdala.9 As shown by Elizabeth Phelps of NYU, such “fear conditioning” occurs faster for other-race than same-race faces. Amygdalae are prepared to learn to associate something bad with Them. Moreover, people judge neutral other-race faces as angrier than neutral same-race faces.
So if whites see a black face shown at a subliminal speed, the amygdala activates.10 But if the face is shown long enough for conscious processing, the anterior cingulate and the “cognitive” dlPFC then activate and inhibit the amygdala. It’s the frontal cortex exerting executive control over the deeper, darker amygdaloid response.
Second depressing finding: subliminal signaling of race also affects the fusiform face area, the cortical region that specializes in facial recognition.11 Damaging the fusiform, for example, selectively produces “face blindness” (aka prosopagnosia), an inability to recognize faces. Work by John Gabrieli at MIT demonstrates less fusiform activation for other-race faces, with the effect strongest in the most implicitly racist subjects. This isn’t about novelty—show a face with purple skin and the fusiform responds as if it’s same-race. The fusiform isn’t fooled—“That’s not an Other; it’s just a ‘normal’ Photoshopped face.”
In accord with that, white Americans remember white better than black faces; moreover, mixed-race faces are remembered better if described as being of a white rather than a black person. Remarkably, if mixed-race subjects are told they’ve been assigned to one of the two races for the study, they show less fusiform response to faces of the arbitrarily designated “other” race.12
Our attunement to race is shown in another way, too.13 Show a video of someone’s hand being poked with a needle, and subjects have an “isomorphic sensorimotor” response—hands tense in empathy. Among both whites and blacks, the response is blunted for other-race hands; the more the implicit racism, the more blunting. Similarly, among subjects of both races, there’s more activation of the (emotional) medial PFC when considering misfortune befalling a member of their own race than of another race.
This has major implications. In work by Joshua Correll at the University of Colorado, subjects were rapidly shown pictures of people holding either a gun or a cell phone and were told to shoot (only) gun toters. This is painfully reminiscent of the 1999 killing of Amadou Diallo. Diallo, a West African immigrant in New York, matched a description of a rapist. Four white officers questioned him, and when the unarmed Diallo started to pull out his wallet, they decided it was a gun and fired forty-one shots. The underlying neurobiology concerns “event-related potentials” (ERPs), which are stimulus-induced changes in electrical activity of the brain (as assessed by EEG—electroencephalography). Threatening faces produce a distinctive change (called the P200 component) in the ERP waveform in under two hundred milliseconds. Among white subjects, viewing someone black evokes a stronger P200 waveform than viewing someone white, regardless of whether the person is armed. Then, a few milliseconds later, a second, inhibitory waveform (the N200 component) appears, originating from the frontal cortex—“Let’s think a sec about what we’re seeing before we shoot.” Viewing a black individual evokes less of an N200 waveform than does seeing someone white. The greater the P200/N200 ratio (i.e., the greater the ratio of I’m-feeling-threatened to Hold-on-a-sec), the greater the likelihood of shooting an unarmed black individual. In another study subjects had to identify fragmented pictures of objects. Priming white subjects with subliminal views of black (but not white) faces made them better at detecting pictures of weapons (but not cameras or books).14
Finally, for the same criminal conviction, the more stereotypically African a black individual’s facial features, the longer the sentence.15 In contrast, juries view black (but not white) male defendants more favorably if they’re wearing big, clunky glasses; some defense attorneys even exploit this “nerd defense” by accessorizing their clients with fake glasses, and prosecuting attorneys ask whether those dorky glasses are real. In other words, when blind, impartial justice is supposedly being administered, jurors are unconsciously biased by racial stereotypes of someone’s face.
This is so depressing—are we hardwired to fear the face of someone of another race, to process their face less as a face, to feel less empathy? No. For starters, there’s tremendous individual variation—not everyone’s amygdala activates in response to an other-race face, and those exceptions are informative. Moreover, subtle manipulations rapidly change the amygdaloid response to the face of an Other. This will be covered in chapter 11.
Recall the shortcut to the amygdala discussed in the previous chapter, when sensory information enters the brain. Most is funneled through that sensory way station in the thalamus and then to appropriate cortical region (e.g., the visual or auditory cortex) for the slow, arduous process of decoding light pixels, sound waves, and so on into something identifiable. And finally information about it (“It’s Mozart”) is passed to the limbic system.
As we saw, there’s that shortcut from the thalamus directly to the amygdala, such that while the first few layers of, say, the visual cortex are futzing around with unpacking a complex image, the amygdala is already thinking, “That’s a gun!” and reacting. And as we saw, there’s the trade-off: information reaches the amygdala fast but is often inaccurate.16 The amygdala thinks it knows what it’s seeing before the frontal cortex slams on the brakes; an innocent man reaches for his wallet and dies.
Other types of subliminal visual information influence the brain.17 For example, the gender of a face is processed within 150 milliseconds. Ditto with social status. Social dominance looks the same across cultures—direct gaze, open posture (e.g., leaning back with arms behind the head), while subordination is signaled with averted gaze, arms sheltering the torso. After a mere 40-millisecond exposure, subjects accurately distinguish high- from low-status presentations. As we’ll see in chapter 12, when people are figuring out stable status relations, logical areas of the frontal cortex (the vmPFC and dlPFC) activate; but in the case of unstable, flip-flopping relations, the amygdala also activates. It’s unsettling when we’re unsure who gets ulcers and who gives them.
There’s also subliminal cuing about beauty.18 From an early age, in both sexes and across cultures, attractive people are judged to be smarter, kinder, and more honest. We’re more likely to vote for attractive people or hire them, less likely to convict them of crimes, and, if they are convicted, more likely to dole out shorter sentences. Remarkably, the medial orbitofrontal cortex assesses both the beauty of a face and the goodness of a behavior, and its level of activity during one of those tasks predicts the level during the other. The brain does similar things when contemplating beautiful minds, hearts, and cheekbones. And assumes that cheekbones tell something about minds and hearts. This will be covered in chapter 12.
Though we derive subliminal information from bodily cues, such as posture, we get the most information from faces.19 Why else evolve the fusiform? The shape of women’s faces changes subtly during their ovulatory cycle, and men prefer female faces at the time of ovulation. Subjects guess political affiliation or religion at above-chance levels just by looking at faces. And for the same transgression, people who look embarrassed—blushing, eyes averted, face angled downward and to the side—are more readily forgiven.
Eyes give the most information.20 Take pictures of two faces with different emotions, and switch different facial parts between the two with cutting and pasting. What emotion is detected? The one in the
eyes.*21
Eyes often have an implicit censorious power.22 Post a large picture of a pair of eyes at a bus stop (versus a picture of flowers), and people become more likely to clean up litter. Post a picture of eyes in a workplace coffee room, and the money paid on the honor system triples. Show a pair of eyes on a computer screen and people become more generous in online economic games.
Subliminal auditory cues also alter behavior.23 Back to amygdaloid activation in whites subliminally viewing black faces. Chad Forbes of the University of Delaware shows that the amygdala activation increases if loud rap music—a genre typically associated more with African Americans than with whites—plays in the background. The opposite occurs when evoking negative white stereotypes with death metal music blaring.
Another example of auditory cuing explains a thoroughly poignant anecdote told by my Stanford colleague Claude Steele, who has done seminal research on stereotyping.24 Steele recounts how an African American male grad student of his, knowing the stereotypes that a young black man evokes on the genteel streets of Palo Alto, whistled Vivaldi when walking home at night, hoping to evoke instead “Hey, that’s not Snoop Dogg. That’s a dead white male composer [exhale].”
No discussion of subliminal sensory cuing is complete without considering olfaction, a subject marketing people have salivated over since we were projected to watch Smell-O-Vision someday. The human olfactory system is atrophied; roughly 40 percent of a rat’s brain is devoted to olfactory processing, versus 3 percent in us. Nonetheless, we still have unconscious olfactory lives, and as in rodents, our olfactory system sends more direct projections to the limbic system than other sensory systems. As noted, rodent pheromones carry information about sex, age, reproductive status, health, and genetic makeup, and they alter physiology and behavior. Similar, if milder, versions of the same are reported in some (but not all) studies of humans, ranging from the Wellesley effect, discussed in the introduction, to heterosexual women preferring the smell of high-testosterone men.
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