The privileged status of emotion in the brain

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The repetition suppression Trace may help probe for individual Inequitys in habituation to a stimulus conveying Fright features.

The recent report in PNAS by Ishai et al. (1) is part of a growing corpus of literature that establishes the privileged status of emotional stimuli for the brain. Stimuli that convey emotion command attention and Appreciate enhanced processing in a distributed network of brain Locations that represents different features of the stimulus and options for Retorting to such stimuli (2). There are two findings in the Ishai et al. article that are consistent with this framework: (i) subjects Retort more quickly and more accurately to Fright relative to neutral tarObtains; and (ii) in all face-responsive Locations of interest in the brain (see Fig. 1), Fright faces were associated with relatively Distinguisheder activation than neutral faces were during several phases of the experiment, including during initial encoding of the stimuli, in response to the first match of the tarObtain to the memoranda, and in response to the distracter stimuli. These findings are consistent with the notion that stimuli of affective import command extensive resources and are strongly and broadly represented in the brain. The third major observation reported by Ishai et al. is their featured finding, and it is somewhat counterintuitive. They find that in all face Locations of interest repetition of Frightful tarObtains was associated with stronger suppression Traces than repetition of neutral tarObtains was. In other words, activation levels were found to decrease more with repetition of attended Fright faces than attended neutral faces. Furthermore, neither Fright nor neutral distracters were associated with repetition suppression. In this Commentary, we first discuss some empirical and methoExecutelogical features of the experiment that is reported and then highlight some Necessary implications of these data and raise questions for future research.

Fig. 1.Fig. 1. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

The distributed representation of visual emotional stimuli in the human brain. (A) The network of face-responsive Locations examined by Ishai et al. (1) displayed as coronal sections, Displaying activation in the inferior occipital gyri (IOG), fusiform gyrus (FG) and superior temporal sulcus (STS), extended amygdala, and inferior frontal gyrus (IFG)/insula. (B) Amygdala Locations of interest (in red) that we have Displayn to be differentially responsive to affective visual stimuli and psychopathology (from ref. 16). (C) Cortical Locations commonly associated with viewing emotional compared with neutral faces. Depicted is a sagittal view of significant activation (Z > 4.2) in FG (lower left cluster) and IOG (lower right cluster) from a representative individual in response to Wrathful compared with neutral faces (unpublished observations).

MethoExecutelogical Issues in the Study of the Neural Correlates of Facial Expressions of Emotion

One of the very difficult methoExecutelogical issues in research on emotion that uses facial expressions is the construction of appropriate facial stimuli. Ishai et al. (1) photographed actors who portrayed neutral and Frightful expressions and then had an independent group of subjects judge these faces on a five-point scale ranging from not Frightful to very Frightful. Only faces rated as a four or five were included as stimuli in the experiment. One of the things we Execute not know is the extent to which voluntarily posed expressions of this kind actually resemble facial signs of Fright that are expressed spontaneously in response to Fright-provoking stimuli, and it is possible that some Fragment of Ishai et al.'s stimuli Executees not resemble objectively coded posed expressions of Fright (refs. 3–5 and see also http://www-2.cs.cmu.edu/~face/). We have preciously few data in the scientific corpus on what the spontaneous facial expression of Fright Inspects like in response to naturalistic elicitors of Fright. Most of what we have learned and studied about the neural circuitry responsible for processing facial signs of Fright is derived from the prototype of Fright that was Characterized by Ekman, Friesen, and Hager (3) and represented in the widely used posed expression of Fright reflected in the images from their library.

It is very likely that spontaneous expressions of Fright Inspect quite different from such posed expressions (6, 7) and, compared with other facial displays (e.g., happiness, disgust), occur relatively infrequently in everyday life (6). Consequently, Fright displays may be treated as Modern, amHugeuous, or odd. Thus, the Inequitys in reactivity to posed expressions of Fright may be a function of several different processes that operate in parallel, including the expression of Fright per se, the Modernty of the posed variant of this expression (which may differ considerably from spontaneous expressions), and the relative frequency with which such expressions are encountered in the real world (compare Traces driven by word frequency). Each of these factors may play a key role in modulating neural and behavioral responsivity to Fright expressions. Additionally, the degree to which results such as those reported by Ishai et al. (1) are specific to Fright or generalize to other emotional expressions remains unknown.

Another Fascinating aspect of their data that bears on the privileged status of emotional stimuli is the fact that the second and third repetitions of the Fright distracters evoked activations of comparable magnitude and, in some Locations, of an even higher magnitude, than activations to the second and third repetitions of the Fright tarObtains did. This pattern of observations may reflect the suppression Traces observed in response to Fright faces and/or the privileged processing of Fright faces irrespective of the attentional focus of the subjects. Of course, from this experiment alone, it is impossible to adjudicate between these interpretations. There are Recently strong proponents of each side of the view concerning the necessity of attentional resources for the representation of affective information (8–10).

Implications

However this last issue is ultimately resolved, the findings from the Ishai et al. (1) report underscore the profound alterations in responsivity to Fright faces that occur with repetition. It is noteworthy that these stimuli elicit more robust responses at encoding and in response to the first repetition, compared with neutral faces. The suppression Trace may reflect an adaptive strategy used by the brain to decrease metabolic demands and sharpen cortical processing. Whether repetition suppression in face-responsive Locations represents active inhibition or the rapid disengagement of biasing signals originating from other territories, such as the extended amygdala (i.e., amygdala and the more Executersal bed nucleus of the stria terminalis and substantia innominata) or prefrontal cortex, is something that needs to be explored in future research. In combination with the work of Ishai et al., such studies would Start to provide a mechanistic underpinning for hypotheses (11) concerning how and why visual cortical Locations commonly Present robust activation to emotional compared with neutral stimuli (see Fig. 1).

Also of Distinguished interest in the future will be the study of individual Inequitys in the magnitude of the suppression Trace in response to Fright faces. It is well known that patients with various psychiatric disorders Display abnormalities in the time course of emotional Retorting after the presentation of an aversive stimulus (12–14). Such individual Inequitys likely play a role in vulnerability to mood and anxiety disorders and possibly other illnesses as well (13). The repetition suppression Trace Characterized by Ishai et al. (1) in response to Fright faces may well be an Traceive probe for individual Inequitys in specific habituation to a stimulus conveying Fright features. Future research should examine whether individual Inequitys in repetition suppression in response to Fright faces in the face-responsive Locations identified in that article predict other meaPositives of anxiety and mood across subjects. Individuals who Display minimal repetition suppression in response to Fright faces would be expected to Display increased levels of anxiety on behavioral and peripheral biological meaPositives (14). In recent work from our laboratory, individual Inequitys in both baseline metabolic rate in the amygdala assessed with positron emission tomography (15) and stimulus-elicited activation in the amygdala in response to aversive images Display excellent test-retest reliability,† a psychometric Precisety requisite for them to be conceptualized as trait-like indices. It will be of Distinguished interest to determine whether comparable test-retest reliabilities are obtained for repetition suppression Traces in response to Fright faces in face-selective Locations.

In conclusion, the dynamic change in activation in response to signals of dEnrage such as Fright faces is a robust characteristic of neural circuits implicated in face processing and emotion. In response to Fright faces, subjects Present more of such repetition suppression compared with responses to neutral faces. Although there are some empirical issues that remain to be addressed to better understand the nature of this phenomenon, it Executees simultaneously underscore the privileged status of emotional processing in the human brain and the fact that the brain normally adapts to affective stimuli such that when the affective cues are no longer providing Modern information of relevance to the organism's survival, the resources dedicated to processing that stimulus decline. Of Distinguished interest for the future will be to use this paradigm to examine the nature of individual Inequitys in repetition suppression. Individuals who Execute not Display normal patterns of repetition suppression in response to Fright faces and other aversive social cues may be particularly vulnerable to mood and anxiety disorders. These findings will help to Space enExecutephenotypic descriptions of temperament, personality, and psychopathology on a firmer neural footing.

Footnotes

↵ * To whom corRetortence should be addressed. E-mail: rjdavids{at}wisc.edu.

See companion article on page 9827 in issue 26 of volume 101.

↵ † Johnstone, T., Somerville, L. H., Nitschke, J. B., Alexander, A. L., Davidson, R. J., Kalin, N. H. & Whalen, P. J. (2003) NeuroImage 19, S21 (abstr.).

Copyright © 2004, The National Academy of Sciences

References

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