Recognition of facial emotion in nine individuals with bilateral amygdala damage

doi:10.1016/S0028-3932(99)00039-1

Neuropsychologia

Volume 37, Issue 10, September 1999, Pages 1111-1117

https://doi.org/10.1016/S0028-3932(99)00039-1 Get rights and content

Abstract

Findings from several case studies have shown that bilateral amygdala damage impairs recognition of emotions in facial expressions, especially fear. However, one study did not find such an impairment, and, in general, comparison across studies has been made difficult because of the different stimuli and tasks employed. In a collaborative study to facilitate such comparisons, we report here the recognition of emotional facial expressions in nine subjects with bilateral amygdala damage, using a sensitive and quantitative assessment. Compared to controls, the subjects as a group were significantly impaired in recognizing fear, although individual performances ranged from severely impaired to essentially normal. Most subjects were impaired on several negative emotions in addition to fear, but no subject was impaired in recognizing happy expressions. An analysis of response consistency showed that impaired recognition of fear could not be attributed simply to mistaking fear for another emotion. While it remains unclear why some subjects with amygdala damage included here are not impaired on our task, the results overall are consistent with the idea that the amygdala plays an important role in triggering knowledge related to threat and danger signaled by facial expressions.

Introduction

Studies in animals have demonstrated the amygdala’s importance in behaviors elicited by stimuli with high emotional significance. Recently, the amygdala’s role has also been explored in humans, using both the lesion method and functional imaging. Several reports found that bilateral damage to the human amygdala impairs the recognition of emotions in facial expressions, especially in the case of fear [6], [7], [12], [13], [25], [26]. Similarly, functional imaging studies have found activation of the amygdala when viewing facial expressions of fear, as compared to neutral faces [11], [19], [20], [21], even under conditions of subliminal presentation [24]. These studies provide strong support for the idea that the amygdala, in humans as in animals, plays a key role in triggering behaviors and knowledge retrieval in response to biologically salient stimuli, especially those related to possible danger and threat.

However, comparisons between different studies have been difficult, because different sets of stimuli, and different methods, have been used. For example, several studies by Young and colleagues [12], [13], [25], [26] have used certain sets of face stimuli, and a labeling task, whereas other studies [6], [7], [15] have used a different set of stimuli and a task in which subjects’ ratings were correlated with normal ratings. Moreover, the study by Hamann et al. [15] reported intact recognition of facial emotion in two subjects with complete bilateral amygdala damage.

The present report is a collaboration between all the different laboratories that have published data on facial emotion recognition in subjects with bilateral amygdala damage, with the aim of examining subjects from several research groups on the same task, so as to permit direct comparisons. We report findings from six individuals who have been described in prior reports, and from three whose facial recognition was studied here for the first time. All nine subjects were administered identical stimuli in an identical task that provided a detailed and quantitative assessment of their ability to recognize emotion in facial expressions (identical to that used in [6], [7], [15]). We addressed the following specific issues:

1.
We re-investigated the hypothesis that bilateral amygdala damage would impair the recognition of fear in facial expressions by comparing the group of nine individuals with bilateral amygdala damage with a group of 16 brain-damaged controls, all tested on the same task. This provided sufficient power to permit a direct statistical test of the hypothesis.
2.
We further hypothesized that impairments in recognizing facial emotion would not be restricted to fear, but rather would encompass a class of emotions related to threat and danger. Again, our sample size permitted a statistical test of this possibility.
3.
Finally, we wished to explore the reasons that individuals with bilateral amygdala damage might be impaired in recognizing facial emotion. In particular, did they consistently mistake one facial emotion for another, or did they simply give a more inconsistent performance on certain facial emotions? To determine performance consistency, a subset of subjects participated in replications of the experiment.

Section snippets

Target subjects

Neuroanatomical data on all individuals with bilateral amygdala lesions included in this study have been described previously. A summary of their etiology and background biographical information is given in Table 1. Subjects SM [6], [7], EP and GT [15] have previously been tested on the same task used here; SP has been tested on a subset of the stimuli with an identical analysis [9], [10]. Subjects DR and SE [13], [25], [26] have previously been tested on different tasks requiring choice of

Results

The raw data for the group of seven normal controls, the 16 brain-damaged controls, and eight of the nine individuals with bilateral amygdala damage are shown in Fig. 1. (SP’s raw data are not shown in the figure. This subject was not administered a complete set of stimuli, and we wished to avoid uneven weighting of different stimuli.) Normal and brain-damaged controls gave very similar performances, as indicated by the nearly identical data graphs. By contrast, subjects with bilateral amygdala

Discussion

This study provided a unique opportunity to compare a relatively large number of rare individuals with bilateral amygdala damage (N=9) on a single, standardized task. The findings permit some conclusions that have not been possible from prior reports that studied subjects separately.

On the basis of previous lesion and functional imaging studies, we had hypothesized that bilateral damage to the human amygdala would impair the recognition of fear in facial expressions. An examination of this

Acknowledgements

We thank Larry Squire for making subjects EP and GT available, and for comments on the manuscript. We thank Denise Krutzfeldt for help with scheduling subjects, and Kristofer Kinsey and Jeremy Nath for help with testing. Supported in part by NINDS grant NS19632 and a grant from the Mathers Foundation (A.R.D.), a Sloan Foundation Fellowship and NIMH grant MH57905 (R.A.), the U.K. Medical Research Council (A.W.Y. and A.J.C.), and NIMH grant R29-MH50812 (E.P.).

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Recognition of facial emotion in nine individuals with bilateral amygdala damage

Abstract

Introduction

Section snippets

Target subjects

Results

Discussion

Acknowledgements

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