Learning to fear what others have feared before.
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ABSTRACT: The ability to recognize facial emotions is altered in patients with Bipolar Disorder (BD) during mood episodes and even in euthymia, while cognitive functioning is similarly impaired. This recognition is considered a fundamental skill for successful social interaction. However, it is unclear whether the ability to recognize facial emotions is correlated with the cognitive deficits observed in BD. The objective of this study was to evaluate Facial Emotion Recognition (FER) and its correlation with executive function (EF) in BD I patients during mania, depression and euthymia compared to healthy controls. A total of 110 patients with BD I, 18-40 years old were included (41 in manic episode; 31 in depressive episode and 38 euthymic). Patients were assessed for FER and EF (Wisconsin card sorting test - WCST), along with 96 healthy volunteers (18-40 years old) recruited from the University of São Paulo. The results showed that BD I patients had lower FER performance compared to controls on fear subtests, happiness, the surprise test, and FER total scores. Moreover, BD I manic patients showed poorer performance for EF compared to controls. Six out of the seven variables of the WCST correlated with FER in both healthy controls and BD euthymic subjects but not in BD patients during mood episodes. Cognitive deficits and difficulties recognizing facial emotions are present in all mood episodes in BD I patients, even during remission. Although FER is not considered a cognitive domain, these results suggest that, along with EF, it has a complementary function. Hence, further studies should investigate this issue in larger samples and verify whether these similarities also occur at a neurobiological level.Journal of Affective Disorders 10/2013; · 3.76 Impact Factor
In this Issue
Learning to fear what others have feared before
Humans, like most organisms, are built to learn what may
cause us harm so that we avoid it in the future. I learned the
the burner of an electric stove just after it had been turned off.
As I touched the burner I noticed a light illuminated on the
stove panel, thereby learning to associate the panel light with
the potential for a painful burn. For many weeks after my
painful initiation to the ways of electric stoves the sight of the
panel light made me feel apprehensive and wary.
This simple, but essential, form of associative learning has
for decades been studied using the conditioned fear (CF)
paradigm in which participants learn to ‘fear’ a previously
neutral stimulus (the conditioned stimulus or CSþ, e.g. a
simple shape or stove panel light) through its repeated
pairing with an intrinsically aversive stimulus (the uncondi-
tioned stimulus, or UCS, e.g. a mild shock, or in my case, a
hot burner). Over time, presentations of the CSþ alone
comes to elicit responses like those initially elicited only by
the UCS (e.g. a transient rise in skin conductance). In recent
years, the CF paradigm has been a powerful tool in both
animal and human studies for elucidating the neural systems
supporting learning to ‘fear’ that which may cause us harm.
emerged as the key site for forging the link between stimuli
and their potentially aversive consequences (LeDoux, 2000).
Learning through direct experience is not, however, the
only or even most common way we learn what has threat
value. Indeed, the friends who watched me touch the stove
did not need to repeat my mistake in order to know the
meaning of an illuminated panel light. This ability to learn
vicariously from the actions of others has been captured by
the observational fear (OF) paradigm, in which an individual
watches another person undergo the CF procedure.
Although studies in both animals and humans have shown
OF and CF learning may show similar behavioral character-
istics (Olsson and Phelps, 2004), until now, no studies had
addressed the underlying neural mechanisms.
In this issue, Olsson and Phelps report the first functional
imaging study of OF learning. Using a human analog of a
behavioral paradigm first developed in animal studies,
Olsson and Phelps scanned participants both while watching
a video clip of an individual in a CF experiment and
afterwards during presentations of the CSþ and a control
CS? that had not been paired with shock in the video.
Strikingly, amygdala activity was observed both during
observational learning and during expression of a CR.
This result is important for at least five reasons. First, it
provides the first examination of the neural systems involved
in a form of social, vicarious learning. Second, it demonstrates
a viable method for studying social learning that could be
adapted for addressing various questions about how we learn
from others. Third, it demonstrates that vicarious learning of
fear may rely upon mechanisms like those involved in learning
to fear through direct experience, thereby joining a growing
literature suggesting that common or shared representations
support the direct perception of pain, emotion or action as
well as the perception of the same in other people (Wicker
et al., 2003; Singer et al., 2004; Decety and Grezes, 2006).
Fourth, Olsson and Phelps observed activity during observa-
tional learning in a network of brain systems not typically
associated with CF learning, but rather associated with social
cognition, including medial prefrontal cortex and the superior
temporal sulcus (Gallagher and Frith, 2003). Although activity
in these regions previously has been associated with drawing
inferences about the mental states of others, and taking their
third person perspective, this is the first study to show that
these regions may play a role in learning. Fifth, it highlights
the usefulness of animal models for social cognitive and
affective neuroscience research. The OF paradigm used by
Olsson and Phelps used methods similar to those used in
animal models of observational learning, that in turn were
based upon animal models of conditioned fear (Mineka and
Cook, 1993). Cross-species comparisons may both illuminate
underlying mechanisms and highlight what is unique about
vicarious learning in humans.
That being said, by taking steps in new directions, the
present experiment?like any impactful study?may raise more
interesting questions than it answers. Perhaps foremost among
them is the question of what specific roles in observational
learning are played by the various neural systems activated in
addition to the amygdala, and what factors mediate the learn-
ing of observational fear. Now that we know it depends upon
activity both in the amygdala and regions involved in social
cognition, the question naturally arises as to what role social
cognition plays in OF learning. Might perspective taking, for
example, play an essential role in this learning, supported by
activity in regions associated with mental state inference, and
could activity in these regions mediate amygdala-based fear
learning? Other questions concern the generalizability of the
effects observed here?would other forms of vicarious or obser-
vational learning depend upon the specific systems identified
here, and/or more generally follow the principles observed here
doi:10.1093/scan/nsm007SCAN (2007) 2,1–2
? TheAuthor (2007).Publishedby OxfordUniversityPress.For Permissions,pleaseemail:email@example.com
and in other studies of shared representations?i.e. will similar
systems always support direct and vicarious learning?
Whatever the answers to these specific concerns and
questions, it is clear that part of what makes this study
important, and a likely citation classic, is its Homer
Simpsonesque, ‘Doh!’ factor. Upon hearing about the study
and its results, we might immediately make this exclamation
and wish we had thought of doing it ourselves. May we all
learn through observation to conduct studies of similar impact.
Department of Psychology
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New York, NY 10027
Decety, J., Grezes, J. (2006). The power of simulation: imagining one’s own
and other’s behavior. Brain Research, 1079, 4–14.
Gallagher, H.L., Frith, C.D. (2003). Functional imaging of ‘theory of mind’.
Trends in Cognitive Science, 7, 77–83.
LeDoux, J.E. (2000). Emotion circuits in the brain. Annual Review of
Neuroscience, 23, 155–84.
observational conditioning of fear. Journal of Experimental Psychology
General, 122, 23–38.
Olsson, A., Phelps, E.A. (2004). Learned fear of ‘‘unseen’’ faces after
Pavlovian, observational, and instructed fear. Psychological Science, 15,
Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R.J., Frith, C.D.
(2004). Empathy for pain involves the affective but not sensory
components of pain. Science, 303, 1157–62.
Wicker, B., Keysers, C., Plailly, J., Royet, J.P., Gallese, V., Rizzolatti, G.
(2003). Both of us disgusted in My insula: The common neural basis of
seeing and feeling disgust. Neuron, 40, 655–64.
2 SCAN (2007)Kevin Ochsner