Saturday, July 30, 2005

Fear, Race, and the Unconscious

The amygdala is an often misunderstood brain region. It's closely associated with emotion in general, as well as many emotionally-mediated cognitive and perceptual processes, including face recognition and even affect-mediated memory recall. Despite its many functions, it's often treated in casual discussions and the popular press as the source of one particular emotion: fear. For example, in the recent discussion of the neuroimagining studies of males and females during orgasm, the fact that deactivation was observed in the amygdala was discussed almost exclusively as a decreased fear response, even though there's no other evidence (e.g., in the form of skin conductance responses) that fear responses were decreased. It's dangerous, then, to talk about fear and the amygdala in relation to certain controversial topics. But dangerous is my middle name (seriously, it's on my birth certificate), so I'm going to chance it anyway. Readers should keep in mind the difficulty in interpreting results associated with neuroimagining data indicating increased (or decreased) activation in areas with multiple functions.

While the amygdala is associated with many emotions, there is growing evidence that it is closely associated with fear and fear-related conditioning in nonhuman animals and humans. First, while bilateral damage to the amygdala produce general emotional deficits in humans1, bilateral amygdala lesions are specifically associated with deficits in fear conditioning and produce severe deficits in the recognition of fearful faces2 and vocal intonation3 associated with fear relative to deficits in recognizing those displaying or expressing other emotions (e.g., happiness). Several imaging studies have also observed increased amygdala activation during fear conditioning4, as well as the recognition of fearful faces5, and the visual or cognitive6 representation of fearful stimuli. It's pretty clear, then, that the amygdala is a central part of the system that produces fear recognition and conditioning in humans.

Another line of research, born of the controversy surrounding the claim that the Implicit Association Test (IAT) may reveal implicit racial attitudes, has investigated the neural activity underlying such attitudes. In one study7, researchers presented participants with photos of unfamiliar white and black faces while they were in an fMRI machine. They also gave the participants the IAT, as well as another implicit measure (startle eyeblink), and asked them to describe their attitudes toward African Americans. They found that activation in the amygdala increased for black faces, and was correlated with implicit attitudes (more activation in the amygdala corresponded to more negative associations with African Americans), but not with explicitly expressed attitudes8.

A second study presented white and black participants with photos of white and black faces while they were in an fMRI, and measured amygdalar activation over time9. For ingroup faces (white faces for white participants, black faces for black participants), amygdala activation decreased over time as several ingroup faces were viewed. For outgroup faces, no such decrease in activation was observed. Thus, after the presentation of several ingroup and outgroup faces, amygdala activation was low for ingroup faces but high for outgroup faces.

In a third imaging study, participants were again presented with white and black faces, this time for two different durations, short (30ms) and long (525 ms)10. This study also showed higher amygdala activation for black faces than white faces for white participants, but only for the short durations. At longer durations, there was no difference in amygdala activation between white and black faces, while there was increased activation for black faces in cortical areas associated with conscious control. The researchers argue that this explains the findings from the first study, claiming that initially, implicit attitudes are activated, but longer exposure allows conscious, or explicit attitudes to be activated and to inhibit the implicit associations.

OK, so I told you all of that to tell you about this. These three studies indicate that the processing of faces from members of racial outgroups results in activation in the amygdala. This may indicate that fear responses and racial attitudes share neural systems. There is in fact some behavioral evidence for this. According to terror management theory, which has produced a ton of supporting data over the last decade or so, fear (especially fear of death), produces exaggerated ingroup-outgroup responses11. In particular, negative evaluations of outgroup members are heightened, as are positive evaluations of ingroup members. These findings motivated a just-published study on the relationship between fear conditioning and racial attitudes12. The researchers presented white and black participants with white and black faces, as in the imaging studies, but added a twist. During the presentation of either the black or white faces (varying which face across participants), the participants also received a mild electric shock. After a few trials, they exhibited a conditioned response (measured by skin conductance) to the faces associated with the shock, but not to the faces that were not associated with a shock. After the conditioning phase, the participants were again presented with the faces, but without any shock. The result of interest was the extinction rates for ingroup vs outgroup faces. For some stimuli (the researchers mention snakes and spiders), fear responses seem to elicit prepared conditioning responses, so that when those stimuli are paired with an aversive experience (like electric shocks), extinction takes longer than it does for stimuli that aren't preconditioned to be associated with fear (they use butterflies and birds). If the extinction of conditioned fear responses take longer for racial outgroup faces than for ingroup faces, it would indicate that there is a preconditioned association with fear for those faces. This is in fact what they found: for white participants, the fear responses took significantly longer to extinguish for black faces than white faces, and the opposite was observed for black participants. The only participants who didn't, on average, show this effect were those who had a lot of interracial dating experience (i.e., positive experience with racial outgroup members).

All of this information taken together presents a fairly clear picture: fear and negative racial attitudes are closely associated. However, the authors of the last study make it clear that they don't believe their data implies an innate fear of racial outgroup members, as some have argued such prepared responses to snakes, spiders, and other fear-related stimuli indicate. Here is how they put it:
In other words, because of its relatively recent emergence as an important dimension in human social interaction, race inherently cannot be the basis of the outgroup preparedness result. Instead, it is likely that sociocultural learning about the identity and qualities of outgroups is what provides the basis for the greater persistence of fear conditioning involving members of another group. Most notably, individuals acquire negative beliefs about outgroups according to
their local cultures, and few reach adulthood without considerable knowledge of these prejudices and stereotypes. It is plausible that repeated exposure to information about outgroups might prepare individuals to fear newly encountered outgroup members.
Studies like these will can help people in combating negative racial attitudes. The empirical evidence I've discussed here shows that conscious attitudes can inhibit implicit (likely unconscious) negative racial attitudes, and that positive exposure to members of racial outgroups (as in those participants who had interracial dating experience in the last study) can create positive implicit attitudes towards the members of other races. This means that people are less likely to act on implicit negative attitudes towards members of other races when they have the time and cognitive resources to allow their explicit attitudes to take control. It also means that negative associations can be combated through positive exposure to members of other races. In other words, diversity is important, because it allows for positive exposure to the members of other races. Hopefully future research will find other ways to diminish the fear-related emotional responses to other races as well.

1 Aggleton, J.P. (1992). The functional effects of amygdala lesions in humans: A comparison with findings from monkeys. In J.P. Aggleton (ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wilely-Liss, 485-503.
2 Calder, A.J., Young, A.W., Rowland, D., Perrett, D.I., Hodges, J.R., Etcoff, N.L. (1996). Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cognitive Neuropsychology, 13, 699-745.
3 Scott, S.K., Young, A.W., Calder, A.J., Hellawell, D.J., Aggleton, J.P., Johnson, M. (1997). Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature, 385(6613), 254-257.
4 Quirk G.J., Armony, J.L. & LeDoux, J.E. (1997). Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala. Neuron, 19, 613-624; LaBar, K.S. Gatenby, J.C., Gore, J.C., LeDoux, J.E., & Phelps, E.A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: a mixed trial fMRI study. Neuron 20, 937-945.
5 Morris, J.S., Frith, C.D., Perrett, D.I., Rowland, D., Young, A.W., Calder, A.J., Dolan, R.J. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions.
6 Phelps, E.A., O'Connor, K.J., Gatenby, C., Gore, J.C., Grillon, C., & Davis, M. (2001). Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience, 4, 437-441.
7 Phelps, E.A., O'Connor, K.J., Cunningham, W.A., & Funayama, E.S. (2000). Performance on indirect measures of race evaluation predicts amygdala activation. Journal of Cognitive Neuroscience, 12(5), 729-738.
8 Interestingly, in their second experiment, they used familiar (famous) and positively regarded black faces. In this case, they didn't observe increased amygdalar activation to black faces. This confirms the "safe black person" phenomenon that is so common these days.
9 Hart, A.J., Whalen, P.J., Shin, L.M., McInerney, S.C., Fischer, H., & Rauch, S.L. (2000). Differential response in the human amygdala to racial outgroup vs ingroup face stimuli. NeuroReport, 11(11).
10 Cunningham, W.A., Johnson, M.K., Raye, C.L., Gatenby, J.C., Gore, J.C., & Banaji, M.R. (2004). Separable neural components in the processing of black and white faces. Psychological Science, 15(12), 806-813.
11 Solomon, S., Greenberg, J., Schimel, J., Arndt, J., & Pyszczynski, T. (in press). Human awareness of death and the evolution of culture. In M. Schaller and C. Crandal (eds.), The psychological foundations of culture. Erlbaum.
12 Olsson, A., Ebert, J.P., Banaji, M.R., & Phelps, E.A. (2005). The role of social groups in the persistence of learned fear. Science, 309, 785-787.


Brandon said...

Yet another reason for something like Bullworth's "open-ended program of procreative racial deconstruction"!

Blar said...

Is it possible that the extinction results are due to familiarity? I'm thinking of an explanation like this: People who have a lot of prior experience with some type of stimulus with which they have a few aversive experiences do not develop as strong of a conditioned response as people with less prior experience. Since people have more prior experience with same-race people (with a few exceptions, like those who have dated interracially), a negative conditioned response to same-race people is less persistent. Is there something about the process of fear conditioning or the results of the Olsson et al. study that rules out this alternative account?

Chris said...

Blar, there is some evidence that simple familiarity can't explain it. I didn't describe all of the correlations that they looked at, and only mentioned the interracial dating factor because it was the only one with a strong negative correlation with the time to extinction. They also included friendship, acquaintances, and a implicit and explicit measures of racial attitudes. The number of interracial friends and acquaintances that a person had didn't correlate with conditioning at all, indicating that simple exposure or familiarity wasn't sufficient to explain the data.

Of course, that doesn't completely rule out familiarity. It will take future research to fully explain the data, though all of the experiments placing reactions to racial outgroup members and fear conditioning in the same brain area are pretty suggestive. Of course, that's why I included the warning at the beginning: they're suggestive, but not conclusive.

Anonymous said...

You said:
"positive exposure to members of racial outgroups (as in those participants who had interracial dating experience in the last study) can create positive implicit attitudes towards the members of other races."

However, correlation does not indicate causation. Not that I necessarily believe this, but perhaps those who choose to date other-race partners may do so because of positive attitudes (and less "fearful" responses) to people of other races.

Chris said...

anon, of course. i didn't mean to imply that the research proved anything, but it certainly suggests something.

Anonymous said...

I'm quite a neophyte in these matters, but it is a topic which facinates me quite a bit. Based on what I've read, and particulary influenced by my reading of Jeff Hawkins' "On Intelligence" I'm beginning to think:

- Pattern recognition and prediction is a foundational principal on which most (upper level, at least) brain activity is built.

- Most interesting aspects of human behavior are triggered by matches or disparities between our current experience (pattern matching) and experience past behavior or innate prejudices (prediction). For example, humor or startled fear when the unexpected happens.

- Face recognition, from what I've read, appears to be a very innate (vs. learned) capability in humans. Just-born babies look deep into the faces of mothers, fathers, and others present and seem to recognize to some extent what they are looking at. Yet they show no fear. It would be interesting to see if there is any different reaction to seeing fair-skinned or dark-skinned faces just after birth and before the constancy of like-skinned familial faces takes effect.

- After repeated experiences of like-skinned faces, a prediction of similar experiences is established. When we see a well-known pattern (such as something resembling a face) that differs remakably from what is expected, it triggers a fear response. For example, a fair-skinned baby born to a fair-skinned family seeing a dark-skinned face would recognize the face, and then recognize that it is different from the faces he knows and expects to see.

- Fear of the differences is built on an animal level response mechanism for survival - those which are different might very well be predators.

- Thus, our prejudices are based on a natural fear of the unknown / different / outsider, but this fear response can be easily overcome with positive and constant experiences. These prejudices are reinforced by society and possible lack of diversity. Prejudices are diminished with repeated positive contra-experiences.

- Other world views, such as the world is a dangerous place or Others can be trusted arise from similar early experiences establishing predictive patterns.

Just some thoughts...

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