Are You Upset? Distinct Roles for Orbitofrontal and Lateral Prefrontal Cortex in Detecting and Distinguishing Facial Expressions of Emotion
Cerebral Cortex December
Are You Upset? Distinct Roles for Orbitofrontal and Lateral Prefrontal Cortex in Detecting and Distinguishing Facial Expressions of Emotion
Ami Tsuchida 0 1
Lesley K. Fellows 0 1
0 The Author 2012. Published by Oxford University Press. All rights reserved. For permissions , please
1 Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University , Montreal, Quebec H3A 2B4 , Canada
Navigating our complex social world requires effective processing of subtle emotional signals, such as those conveyed by facial expressions. Failure to do so may underlie some of the disabling social--emotional deficits common in a range of neuropsychiatric and neurological conditions. Prefrontal cortex (PFC) has long been implicated in these processes, but the particular contributions of subregions within PFC remain unclear. We used a sensitive facial emotion rating task in patients with focal lesions to different regions within PFC to identify distinct contributions of 2 prefrontal regions to recognizing emotions from facial expressions. A combination of region-of-interest and voxel-based lesion--symptom mapping established that damage to ventromedial PFC impaired the detection of subtle facial expressions of emotion. Such patients had difficulty distinguishing emotional from neutral expressions. In contrast, patients with left ventrolateral PFC were able to detect the presence of emotional signals but had difficulty discriminating between specific emotions. These effects were regionally specific: Dorsomedial prefrontal damage had no effect on either aspect of emotion recognition. These findings suggest that separable processes relying critically on distinct regions within PFC responsible, on the one hand, for detecting emotional signals from facial expressions and, on the other, for correctly classifying such signals.
emotion recognition; prefrontal cortex; lesion--symptom mapping
Introduction
The ability to recognize subtle emotions from facial
expressions is crucial for successful social interaction (Haxby et al.
2000). Lesions to the prefrontal cortex (PFC) in general, and
orbitofrontal (OFC) and ventromedial PFC (vmPFC) in
particular, have long been associated with disturbed emotional and
social behavior (Davidson et al. 2000; Stuss and Levine 2002).
There is some evidence that these behavioral problems stem, at
least in part, from deficits in processing basic social and
emotional signals presented by others (Rolls et al. 1994). An
understanding of emotion recognition processes thus has the
potential to inform more precise diagnosis and treatment of
social difficulties related to PFC dysfunction. Such insights may
also provide a brain-based framework for understanding
social-emotional deficits in neuropsychiatric conditions, such as
autism.
Functional neuroimaging (Wager et al. 2003; Fusar-Poli,
Placentino, Carletti, Allen, et al. 2009) and lesion studies
(Adolphs et al. 2000; Philippi et al. 2009) have implicated
a number of cortical and subcortical structures in the
recognition of emotion from facial expressions. While the
roles of posterior brain regions and the amygdala have been
studied in considerable detail (Adolphs 2002), the
contributions of specific regions within PFC to emotion recognition
remain a matter of debate. While human lesion studies have
focused primarily on vmPFC and OFC, functional neuroimaging
studies suggest that other PFC regions are involved: A recent
meta-analysis reported consistent activations in bilateral
ventrolateral and dorsomedial PFC (dmPFC) across functional
neuroimaging studies of various emotional face recognition
tasks in healthy subjects (Fusar-Poli, Placentino, Carletti, Allen,
et al. 2009).
Given the potential complexity of the processes triggered by
emotional stimuli, loss-of-function studies are important in
defining the necessary contributions of particular brain regions
at the component process level. The functional neuroimaging
literature raises the possibility that the vmPFC/OFC focus of PFC
lesion studies to date has been overly narrow. Furthermore, even
those studies, in aggregate, are inconclusive, with some finding
that damage to this region results in impaired identification of
facial emotional expressions (Hornak et al. 1996; Heberlein et al.
2008), and others failing to detect effects specific to vmPFC
(Hornak et al. 2003; Shamay-Tsoory et al. 2003).
This literature is complicated by the use of different tasks
and stimuli. In particular, the forced-choice labeling tasks used
in most of the above studies do not differentiate between
deficits in detecting emotional signals in general or in
discriminating between specific emotions. Also, such tasks
typically do not control for differences in confusability
between the 6 cardinal emotions typically studied (e.g., forced
choice between fear and happiness is easier than between fear
and surprise) (Adolphs 2002). Facial emotion rating tasks are
one solution to these (...truncated)