"They are lasting effects." Adds Plotsky, "you can do something fairly mundane in the first days of the animal's life, and somehow this changes how that animal responds to its environment for the rest of its life."

Tracing temperament

But it's not only environmental effects—both extreme and subtle—that color emotional responses. Studies in both animals and humans support the idea that individuals carry certain dispositions throughout their lives. For example, Kalin has found that some infant monkeys are abnormally fearful, exhibiting a startled "freeze" behavior with very little provocation and having high baseline cortisol levels. And in humans, decades of study by Harvard University psychologist Jerome Kagan and his colleagues are revealing what look like innate, lifelong temperaments. Kagan's group examined 450 baby boys and girls, first at 16 weeks, then again at 14 months, 21 months, 4 years, and 7 years, by testing their response to cues they could see, hear, and smell, such as a cotton swab dipped in alcohol.

They found that 20% of the 16-week old infants fell into a test category Kagan calls "high reactive": The tests made them fretful and agitated. Another 35% responded with little distress and low motor activity. Over time, some of the high reactives began to respond normally, while others began to show extreme shyness. None became a bold, fearless child, says Kagan. By age 7, about one-third of the high reactives had developed extreme fears compared with 10% of the others, Kagan said at the NIMH meeting.

Brain imaging complements these behavioral studies by showing a consistent package of brain activation that dovetails with temperamental differences. In Kalin's study, the abnormally fearful rhesus monkeys also had relatively more right frontal brain activity, as recorded by electroencephalograms.

Davidson finds a similar asymmetry in people. People who are negative or depressed according to standardized psychological tests tend to show more baseline prefrontal activity on the right, he says. And the happy-go-lucky folks who are more likely to bounce back when life throws a curve ball tend to show more activity in the left prefrontal cortex.

He speculates that the prefrontal cortex modulates the emotional activity of the amygdala. People with more left prefrontal cortex activity can shut off the response to negative stimuli more quickly, he says. "Being able to shut off negative emotion once it's fumed on is a skill that goes with left activation." He adds that it's not yet known whether such temperaments are in born or a product of very early life experiences.

Indeed, Davidson and others caution that they have far to go in explaining the full biological basis of our passions. LeDoux calls the state of the science of emotions "infantile," as the only emotion for which the neural hardware and software is well understood is fear, and even that has mostly been parsed in the rat. "Things have not entirely coalesced into a coherent picture," agrees NIMH director Steve Hyman. He hopes to help it develop, by pushing neuroimagers to test hypotheses about the neural circuits, and by "goosing cognitive neuroscience to start considering emotion." Darwin would no doubt approve and sympathize. Understanding the origin of emotional expressions remains a great difficulty, he wrote, and "it deserves still further attention."

-Christine Mlot

Christine Mlot is a science writer in Madison, Wisconsin.

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Unmasking the Emotional Unconscious

What—or where—is the unconscious mind? That question has long been the province of psychotherapists, but now neuroscientists are exploring the nature of awareness (Science, 3 April, pp. 59 and 77), and emotion researchers are joining in. A handful of clever—if controversial—imaging studies offer what may be a glimpse of the elusive unconscious mind at work by revealing different patterns of brain activity when people react to conscious and unconscious emotional stimuli.

Most such emotion studies are based on a method perfected by neuropsychologist Ame Ohman of the Karolinska Institute in Stockholm. Researchers flash a fearful or angry face before subjects for several milliseconds, then flash a neutral face for a longer period. They also measure subjects' skin conductance—a reflection of sweat gland activity and a sign of nervousness. The neutral face apparently masks subjects' awareness of the negative face, as they report seeing only the second image.

But the split-second glimpse of the negative face doesn't go completely unnoticed, as a team led by neuroscientists Paul Whalen and Scott L. Raush of Harvard Medical School and Massachusetts General Hospital in Boston reported in January in the Journal of Neuroscience. They used Ohman's "masking" method while scanning subjects' brains with functional magnetic resonance imaging, which reveals areas of high oxygen uptake. When the fearful face was flashed, the brain showed activity almost exclusively in the amygdala—a structure known to store emotional memory, especially fear. When a positive, happy image was flashed, the signal from the amygdala was reduced, showing that it was less involved.

A new study by Ohman and neuroscientists John Morris and Ray Dolan of University College London adds another twist. Researchers first conditioned subjects by repeatedly showing them the angry face followed by an obnoxious noise, training them, in classic Pavlovian fashion, to have a stronger reaction to the face. Then they did the masking experiment, using positron emission tomography (PET) scans.

The difference in brain activity when the subjects were aware and unaware of the face, Dolan told the O 4th annual Wisconsin Symposium on Emotion last month in Madison, was "dramatic." When subjects did not report seeing the angry I faces, they still registered an increase in skin conductance—and the right amygdala lit up in the PET scan. When subjects were aware of the threatening cues the left amygdala showed activity, suggesting that the left side is involved with conscious response and the right with the unconscious mind.

""What these data are suggesting is that conscious awareness of a target stimulus . . . can modulate the associated neural response,"" Dolan said in his talk. Noting that language is mostly a left-hemisphere function, he speculated that it may help define consciousness.

But others, such as neuroscientist Richard Davidson of the University of Wisconsin, Madison, aren't quite convinced. "I would regard [the finding] as preliminary," he says. "We don't [know] at this point what the neural substrates are of emotional consciousness." Still, he and others are intrigued. What the masking experiments show says Whalen, is that "some part of your body knows that something's out there even when you don't. That's interesting." -C.M.

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