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Disgust discussed.

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Disgust Discussed
Research in the neuropsychology of human emotion
has expanded rapidly in recent years. This is in part
because of the widening availability of functional imaging technology but also because of a newfound interest in the idea that certain individual emotions may
be served by separate neural substrates. This latter theoretical position is at the heart of the basic emotions
concept, the idea that selected emotions with strong
evolutionary histories constitute the foundations of human emotion. Although this concept has its origins in
the work of Charles Darwin,1 it really took off only
after the research of people such as Tomkins, Ekman,
and Izard in 1960s and 1970s. Instead, emotion research up until this point was dominated by the idea
that all emotions were coded as values on a limited
number of dimensions (eg, valence and arousal). Similarly, early neurological accounts of emotion processing took a similar all-encompassing approach in which
all emotions were processed by a circuit of interconnected brain structures such as the limbic system.2– 4
Two important findings of Ekman and his contemporaries that changed theories of emotion were studies
demonstrating that certain emotions were associated
with distinct facial signals and additional research
showing that these facial signals were recognized by
cultures throughout the world, observations that now
form two of the defining features of basic emotions. A
third posited feature was that each basic emotion should
be associated with a distinct (neuro)physiological signature. Although human evidence of this proved difficult
to find, support was found in comparative neuroscience.5,6
Over the last 8 years, human research has similarly
begun to identify that certain emotions may be coded
by partially distinct neural substrates. A good deal of
this evidence has resulted from research aimed at understanding the neural substrates of recognizing emotion in others (ie, the recognition of human signals of
emotion). This work escapes many of the criticisms
leveled at earlier emotion research exploring emotional
experience, such as a reliance on subjective measures
and vague and poorly defined aspects of emotion processing.7 Indeed, neuropsychological investigations of
facial affect recognition have had the added advantage
of being able to build on two established areas of human research—sociocognitive studies of facial expression recognition and neuropsychological research on facial identity recognition.
To date, functional imaging and patient-based research has shown that the human amygdala plays a significant role in recognizing facial and vocal expressions
of fear—an association that concurs with earlier comparative research demonstrating a link between fear
conditioning and the amygdala. Calder and colleagues8
also have recently argued that an additional neural system involving the insula and basal ganglia underlies the
recognition of human signals of disgust. Support for
this position comes from both functional imaging research and neuropsychological studies of brain-injured
patients.8 A particularly striking example comes from a
case (N.K.) with a focal lesion to the left insula and
basal ganglia who demonstrates a highly selective impairment in recognition and experience of disgust.15
However, although these studies demonstrate a link between the insula and disgust, the specific regions of the
insula involved are less clear. On balance functional
imaging research has pointed to the anterior sections of
the insula,9 although not all studies have confirmed
this. In this respect, the study by Krolak-Salmon and
colleagues10 constitutes an important contribution to
understanding which insular regions are involved.
Krolak-Salmon and colleagues recorded event-related
potentials (ERPs) to pictures of facial expressions displaying disgust, fear, happiness, and neutral facial expressions in 11 temporal lobe epilepsy patients with
depth electrode implants in the insular cortex. Significantly, all four patients with electrodes in the anterior
ventral section of the long insular gyrus showed significantly distinct ERPs to facial expressions of disgust.
Moreover, stimulation of the electrodes in three of
these patients caused two to report unpleasant sensations in the throat spreading to the mouth, lips, and
nose, reactions reminiscent of those reported by Penfield and Faulk11 in a similar stimulation study reported some 50 years previously.
Krolak-Salmon and colleagues’ research is informative not only because four proximal electrodes showed
a selective response to disgust, but also because 13 additional electrodes located in more dorsal (mainly posterior) regions of the insula showed no evidence of disgust selectively. The insula constitutes a significant area
of cortex; however, functional imaging studies frequently report signals in this region as simply “insula.”
In addition, stimuli associated with emotions other
than disgust also have been reported to activate the insula in brain imaging research. The study by KrolakSalmon and colleagues emphasizes the need to consider
the insula’s role in emotion processing at a more finegrain level than currently has been applied. The need
for this approach is further substantiated by nonhuman
primate research, showing that the insula is composed
of three distinct regions, agranular, granular, and dys-
© 2003 Wiley-Liss, Inc.
Andrew J. Calder, MD
MRC Cognition and Brain Sciences Unit
Cambridge, United Kingdom
Fig. A sagittal section of Patient N.K.’s8 magnetic resonance
image (MRI), showing the extent of damage to the left insula.
As discussed, Calder and colleagues15 have demonstrated that
N.K. shows a highly selective impairment in recognition and
experience of disgust. His MRI shows damage to the ventral
section of the long insular gyrus; the region that KrolakSalmon and colleagues identified as being selectively responsive
to facial expressions of disgust.
granular. Moreover, it is also relevant that the anteroventral insular area identified by Krolak-Salmon and
colleagues is noted for its role in olfactory and gustatory processing,12 and that lesioning the gustatory insular cortex in rats impairs conditioned taste aversion.13 Finally, it is reassuring that the insular region
identified by Krolak-Salmon and colleagues as being
selectively responsive to disgust (ie, ventral anterior section of the long gyrus) is damaged in Patient N.K.
Although some may be surprised at the idea of a
compartmentalized disgust recognition system in the
human brain, it is important to remember that this
research is still in its infancy. As I have argued elsewhere, evidence consistent with a basic emotions
framework is not inconsistent with a multidimensional
account.14 Hence, whether the ventral anterior insula
turns out to be specific for coding disgust or a more
abstract emotional construct on which disgust weighs
particularly heavily, but not exclusively, remains to be
Annals of Neurology
Vol 53
No 4
April 2003
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DOI: 10.1002/ana.10565
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