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Impaired Judgments of Sadness but Not Happiness Following Bilateral Amygdala Damage

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Impaired Judgments of Sadness but Not Happiness Following Bilateral Amygdala Damage Impaired Judgments of Sadness But Not Happiness Following Bilateral Amygdala Damage Ralph Adolphs* and Daniel Tranel Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/3/453/1758112/089892904322926782.pdf by guest on 18 May 2021 Abstract & Although the amygdala’s role in processing facial expres- damaged and 26 normal controls. Subjects were asked to rate sions of fear has been well established, its role in the the intensity and to label the stimuli. Subjects with unilateral processing of other emotions is unclear. In particular, evidence amygdala damage performed very comparably to controls. By for the amygdala’s involvement in processing expressions of contrast, subjects with bilateral amygdala damage showed a happiness and sadness remains controversial. To clarify this specific impairment in rating sad faces, but performed issue, we constructed a series of morphed stimuli whose normally in rating happy faces. Furthermore, subjects with emotional expression varied gradually from very faint to more right unilateral amygdala damage performed somewhat worse pronounced. Five morphs each of sadness and happiness, as than subjects with left unilateral amygdala damage. The well as neutral faces, were shown to 27 subjects with unilateral findings suggest that the amygdala’s role in processing of amygdala damage and 5 with complete bilateral amygdala emotional facial expressions encompasses multiple negatively damage, whose data were compared to those from 12 brain- valenced emotions, including fear and sadness. & INTRODUCTION such a role (Yang et al., 2002; Breiter et al., 1996). One A number of lesion and functional imaging studies have recent study in fact found amygdala activation (com- demonstrated the amygdala’s role in processing emo- pared with neutral faces) when viewing expressions of tional facial expressions, but its precise importance for fear, anger, sadness, or happiness (Yang et al., 2002). certain emotions remains debated. In particular, while These findings challenge the notion that the amygdala is there are consistent data to implicate the amygdala in specialized to process expressions of fear. perception and judgments of fear (Whalen et al., 2001; It is important to note that the disproportionate Broks et al., 1998; Breiter et al., 1996; Calder et al., 1996; activation to fear compared with other emotions, seen Morris et al., 1996; Adolphs, Tranel, Damasio, & Dam- in most studies, does not rule out some (lesser) activa- asio, 1994, 1995; Adolphs, Tranel, et al., 1999), only tion to other emotions. Thus, activations to emotional some studies have argued also for a role in processing expressions when contrasted with neutral (Yang et al., other negative emotions, especially sadness (Schmolck 2002) may be compatible with activation selectively to & Squire, 2001; Adolphs, Tranel, et al., 1999; Blair, fear, when that emotion is contrasted with any other Morris, Frith, Perrett, & Dolan, 1999). Additional data emotion. One way of investigating these issues would be to suggest that the amygdala may be involved in pro- to parametrically vary the intensity of each emotion using cessing sad expressions come from findings that it is computer-generated morphs between neutral and emo- activated during the feeling of sadness (Schneider et al., tional expressions. Using such morphs might also pro- 1997; Drevets et al., 1992)—although this finding does vide a more sensitive task for detecting possible not demonstrate the amygdala’s involvement in percep- impairments following amygdala damage. Subjects with tion of sadness specifically, it nonetheless suggests that such damage may be able to produce correct perform- abnormal processing related to the emotion sadness ances on some tasks if the stimulus provides a sufficiently may be a feature of amygdala dysfunction (in the same intense prototypical feature—such as a broad smile to way that fear conditioning, phobias, and fear recognition signal happiness (Adolphs, 2002). all depend on the amygdala). While there are no data Clarification of the above controversies would con- from lesion studies to support the idea that the amyg- tribute substantially to the theoretical frameworks used dala is involved in processing happy expressions, some to interpret the data. One view considers the amygdala functional imaging studies have provided evidence for a component of a neural system for the rapid, automatic evaluation of stimuli that signal potential threat or danger in the environment, of which fearful expressions University of Iowa may be signals (Adolphs, Russell, & Tranel, 1999; *Current address: California Institute of Technology. Adolphs, Tranel, et al., 1999). Others view the amygda- D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:3, pp. 453–462 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892904322926782 by guest on 26 September 2021 la’s role as processing signals of distress (Blair et al., control group, comprised by subjects whose brain dam- 1999), thus including fear and sadness, or processing age spared the amygdala. signals that indicate potentially important environmental To obtain a detailed assessment of emotion judgment, information that must be disambiguated (Whalen et al., and to permit comparisons to previous studies, we used 2001), thus pointing to both fear and surprise, and the two tasks that have been most common in the perhaps additional emotions (Yang et al., 2002). Yet literature: rating of the stimulus on all the emotions, other data support the ideas that the amygdala may be and a forced-choice labeling task in which subjects chose more generally involved in withdrawal-related behaviors the word best suited to describe the emotion shown. We (Anderson, Spencer, Fulbright, & Phelps, 2000), which chose our stimuli such that their discriminability from Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/3/453/1758112/089892904322926782.pdf by guest on 18 May 2021 would include multiple negatively valenced emotions, or neutral ranged between 80% and 100%, thus focusing on that it processes the dimension of emotional arousal, stimuli that were just sufficiently different from neutral independently of valence (Anderson et al., 2003). that they could be reliably discriminated most of the These controversies have persisted in part because the time by normal subjects. The accuracy with which the majority of lesion and of functional imaging studies have final set of stimuli can be discriminated from a neutral focused on the amygdala’s role in processing facial face by normal subjects is given in Table 2, together with expressions of fear, and in processing other fear-related the mean rating given to the stimulus on each emotion. information. That role is supported by most of the The mean accuracies in labeling the stimuli by normal studies. By contrast, far fewer studies have systematically subjects are given in Table 3. examined the amygdala’s role in processing other emo- tions. Another reason for the inconsistent findings re- garding the amygdala’s role in judgments of other RESULTS emotions may be that different stimuli and different tasks have been used in various studies. It is thus possible that Ratings Task some studies were simply more sensitive to possible We first asked subjects to rate the morph stimuli on a impairment, whereas others had insufficient sensitivity scale of 1–10 with respect to the intensity of each of the to detect such impairment, or that different tasks and basic emotions. This task has been used in a number of methods of analysis reveal different patterns of impair- prior studies (Schmolck & Squire, 2001; Adolphs et al., ment (Schmolck & Squire, 2001; Rapcsak et al., 2000). 1995; Adolphs, Tranel, et al., 1999), circumvents the To investigate the above issue in more detail, we issue of what emotion response options are available generated morphs between a prototypical neutral ex- to subjects (by explicitly asking them to rate every pression and prototypical expressions of sadness or individual emotion), and provides a fine-grained assess- happiness, thus including stimuli that varied in terms of ment of sensitivity to the intensity of specific individual their sensitivity to judgments of the intended emotion emotions signaled by the face stimuli. (cf. Figure 1). Each of these faint morphs thus generated Subjects with bilateral amygdala damage gave raw a series of (typically monotonically increasing) perform- ratings to several of the sad morphs that were more ances (depicted as the variously colored lines in than 2 SD different from the mean ratings given by brain- Figures 2 and 3). To address the role of the amygdala, damaged controls. Every subject with bilateral amygdala we tested five different subject groups. A normal control damage showed this pattern, and none except AP group was used to provide a reference for all other showed any such impairment for happy morphs. How- comparisons. Subjects with amygdala damage consisted ever, different raw ratings could arise from both an of three groups: those with unilateral left and unilateral impairment in the ability to judge that a morph stimulus right amygdala damage due to neurosurgical temporal was different from a neutral expression, or from differ- lobectomy, and those with bilateral amygdala damage ent baseline ratings for that emotion, even for neutral (Table 1). In addition, we included a brain-damaged stimuli. To take into account subjects’ baseline ratings Figure 1. Examples of morph stimuli
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