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Ralph Adolphs
Division of Humanities and Social Sciences
California Institute of Technology
Pasadena, CA 91125
USA
We often mirror other people's behaviors, and one philosophical and
psychological line of theories (Carruthers and Smith, 1996; Lipps, 1907) has
long proposed that doing so allows us also to mirror other people's minds.
Phenomena such as emotional contagion, imitation and other kinds of mimicry
have been argued to constitute ontogenetic and phylogenetic precursors from
which empathy, simulation and other abilities emerge in adult humans whereby we
gain knowledge about the feelings, intentions and thoughts of others (Meltzoff
and Decety, 2003). Neurobiological and psychophysiological data provide
examples supporting this idea (Blakemore and Decety, 2001; Gallese et al.,
2004; Goldman and Sripada, 2005), but the details remain poorly understood and
the theories remain debated (Adolphs, in press; Jacob and Jeannerod, 2005;
Saxe, 2005).
In a study certain to become a classic, Harrison et al. (page 5) have
demonstrated a role for pupil size in such mirroring. Their data are
impressive: behaviorally, the pupil size of sad faces influences viewers
emotion judgments of the face, even in the absence of explicit awareness of the
observed pupil size; the effect is correlated with regional brain activation of
structures known to mediate emotions; and, perhaps most surprisingly, viewers
own pupils mimic the size of the pupils seen in the sad faces. Taken together,
the findings argue that pupil size is a social signal that can communicate
emotions empathically presumably one that evolved to operate at very close
range.
Pupil size is well-known to be influenced by stimulus luminance, but it turns
out also to be influenced by other factors, including salience and emotional
meaning. Owners of cats will have noticed large changes in their pupil size in
response to stimuli such as a toy mouse or the sound of another cat. Such pupil
changes in humans seem less common in our everyday experience, but may
nonetheless influence our social judgments even when we do not notice them an
effect utilized in the 17th century by women through the use of
atropine-containing eyedrops to dilate their pupils and increase their
perceived attractiveness. As with the present study, it has also been found
that emotional facial expressions in the viewer can be evoked by subliminal
presentation of emotional face stimuli (Dimberg et al., 2000). But the fact
that we have no voluntary control over our pupils makes them an especially good
measure of automatic emotional response, and the short latency of their change
makes this measure in many ways superior to measures such as skin-conductance
response or heart rate in psychophysiology. Aside from its theoretical
importance, the study by Harrison et al. is likely to encourage future
experiments to include pupillometry as a psychophysiological measure, since the
technology to measure pupil size accurately is now widely available even within
the environment of fMRI experiments (as was in fact done in the study).
Several further questions are raised by the findings of Harrison et al. First,
why is the influence of pupil size so specific to sad faces? Effects on happy,
angry or neutral faces were not found. Second, is it pupil size as such or some
other aspect of the eyes that drives the effects reported? One possibility
might be that eyes with smaller pupils would necessarily have larger whites
(the authors digitally adjusted pupil diameter in their stimuli without
altering any other aspects of the eye) and that the slight increase of the area
of the whites of the eyes is responsible for the findings rather than the
slight decrease in the size of the pupils. In line with this alternate
explanation, it has been reported that the amygdala, one of the structures also
found to be activated in the present study, is activated by larger eye whites
that signal fear (Whalen et al., 2004). Future studies could independently
manipulate pupil and scleral size to address this issue.
Finally, the different contrasts and correlations reported in the study raise
the question of what causes what. Perhaps certain brain activations (amygdala
and visual cortices) responded to viewing the sad faces and triggered signals
in the diencephalic autonomic nuclei, which in turn changed the viewer's own
pupil size. However, the change in the viewer's pupil would also result in
different visual input, possibly causing some of the changes in the brain
activation seen. Also notable is that the effect of pupil size on emotion
judgments, and its effect on viewers pupils and brain activations, was carried
out in two separate groups. The subjects in the scanner did not judge the
emotion of the faces. This unfortunately made it impossible to examine possible
relationships between the perceived emotion of the face stimuli and the pupil
size or brain activation of the viewer. Would those subjects showing the
largest responses in their own pupils also make the most sensitive emotion
judgment about the faces they viewed? Such data would help to implicate
causally the pupillary changes in the viewer in influencing emotion judgment.
It would be important to establish the actual distance at which the reported
effects could occur in real life, and the kinds of social interactions that
would predominate at such social distances perhaps especially ones that are
aggressive, maternal or sexual. It remains a puzzle why sadness alone was the
emotion modulated by pupil size in the present study. Presumably, the causal
effects in real life include both viewer and signaler: one could imagine a kind
of positive feedback whereby looking at another person who is sad makes our own
face look sad. These ideas could easily be explored in future experiments, for
instance, by simultaneously monitoring pupil size in two subjects who are
socially interacting at various distances.