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|کد مقاله||سال انتشار||مقاله انگلیسی||ترجمه فارسی||تعداد کلمات|
|37599||2003||9 صفحه PDF||سفارش دهید||محاسبه نشده|
Publisher : Elsevier - Science Direct (الزویر - ساینس دایرکت)
Journal : Neuropsychologia, Volume 41, Issue 10, 2003, Pages 1281–1289
Abstract Bilateral damage to the human amygdala impairs recognition of negatively valenced emotions from facial expressions, but it is unclear if this finding generalizes to richer visual stimuli that contain cues in addition to faces. We investigated this issue in 4 subjects with bilateral amygdala damage, 23 with unilateral amygdala damage, 22 brain-damaged controls and 16 normal individuals. Subjects were shown two blocks of complex social scenes; all stimuli in the two blocks were identical, except that the first block had all facial expressions in the image erased. While control subjects were more accurate in recognizing emotions when facial expressions were present, subjects with bilateral amygdala damage did not show the same benefit for negative emotions, often performing equivalently across the two conditions. Most striking, subjects with bilateral amygdala damage were more accurate in recognizing scenes showing anger with faces erased than with faces present, an effect resulting in part from highly abnormal recognition of certain angry facial expressions. All four subjects with bilateral amygdala damage were impaired in recognizing angry faces shown in isolation, and frequently mistook expressions of anger for smiles, a mistake never made by any control subject. Bilateral amygdala damage thus disproportionately impairs recognition of certain emotions from complex visual stimuli when subjects utilize information from facial expressions
. Introduction Real-life social situations typically provide a rich set of cues that permit viewers to evaluate their emotional significance. The general visual context, the relative locations of people, their body postures, head postures, directions of eye gaze, and facial expressions all provide such cues. This general observation raises two related questions: what is the relative importance of these different cues in recognizing emotions? And are different cues processed by different brain structures? Affirmative answers to both questions are supported in the case of faces: the human face is a particularly salient emotional cue, and there appear to be regions of the brain that are relatively specialized for processing faces. Foremost among these brain regions are sectors of extrastriate visual cortex, notably in the fusiform and superior temporal gyri (Allison, Puce, & McCarthy, 2000; Haxby, Hoffman, & Gobbini, 2000), and the amygdala (Adolphs, 2002). Whereas fusiform and superior temporal cortices may participate primarily in constructing detailed perceptual representations of faces (respectively, of the static, structural configuration, and of the dynamic changes among their features), the amygdala has been shown to be required in order to link the perception of the face to the retrieval of knowledge about its emotional and social meaning (Adolphs, 2002). Ever since the seminal reports of Brown, Shafer, Kluver and Bucy (Kluver & Bucy, 1939), the primate amygdala has been implicated in the regulation of social and emotional behaviors. Lesions of the amygdala in monkeys impair the animal’s ability to evaluate the social and emotional meaning of visual stimuli (Emery et al., 2001; Kling & Brothers, 1992; Meunier, Bachevalier, Murray, Malkova, & Mishikin, 1999; Rosvold, Mirsky, & Pribram, 1954; Weiskrantz, 1956; Zola-Morgan, Squire, Alvarez-Royo, & Clower, 1991). While bilateral lesions of the amygdala in humans appear to have less severe consequences than they do in monkeys, they nonetheless result in alterations in social behavior and social cognition (Adolphs, 1999). Particularly clear is the human amygdala’s role in the recognition of social cues from faces, a role that is best understood in regard to the recognition of basic emotions. Both lesion and functional imaging studies have demonstrated, respectively, impaired recognition of facial expressions following bilateral amygdala damage, and activation of the amygdala during presentation of emotional facial expressions (Adolphs, Tranel, Damasio, & Damasio, 1994; Morris et al., 1996). Notably, these findings are most robust for negatively valenced emotions, in particular fear, anger, and sadness in lesion studies, and fear in functional imaging studies (Adolphs, 1999, Adolphs et al., 1999, Broks et al., 1998 and Calder et al., 1996; Schmolck & Squire, 2001; Young, Hellawell, Van de Wal, & Johnson, 1996), although the reasons underlying these differential patterns of dependency on the amygdala are debated (see Adolphs, 2002 and Rapcsak et al., 2000). The role of the amygdala in processing information about faces is also borne out by single-unit recordings that have found responses relatively selective to faces in both human (Fried, MacDonald, & Wilson, 1997) and non-human primates (Leonard, Rolls, Wilson, & Baylis, 1985). Given the amygdala’s role in recognizing negative emotions from facial expressions when presented in isolation, we wondered if those findings would generalize also to more complex visual social stimuli. Based on the data reviewed above, we hypothesized that the amygdala would be most important to process emotional information from faces, rather than from other visual cues, and that it would be especially important in processing facial expressions of negatively valenced emotions. We thus predicted that damage to the amygdala would yield impaired recognition of such emotions only when the recognition relied on information about facial expressions, and not when it relied on information other than facial expressions. Furthermore, we expected a significant impairment to result from bilateral amygdala damage, but less impairment to result from unilateral amygdala damage, as would be expected and as consistent with prior studies (Adolphs, Tranel, & Damasio, 2001; Adolphs, Tranel, Damasio, & Damasio, 1995; Anderson, Spencer, Fulbright, & Phelps, 2000). To obtain a clear contrast, we investigated the recognition of emotions from two classes of stimuli that were otherwise identical: complex social scenes containing faces, and the same complex social scenes with the faces digitally erased. In all cases, scenes contained multiple visual cues, including body posture, hand gestures, interpersonal stances, and general context, in addition to emotional facial expressions. By directly comparing performances to the scenes when they contained facial expressions, versus when the faces had been erased, we were able to assess the extent to which subjects were able accurately to utilize information from the face in recognizing the emotion signaled by the scene.
نتیجه گیری انگلیسی
Results 3.1. Matching emotions to scenes with faces Across all stimuli, brain-damaged subjects performed, on average, quite comparably to normal controls, yielding mean accuracy scores of 60–70% (chance mean accuracy is at 22%), and performing above chance on every stimulus (Fig. 3, left). Consistent with prior studies in subjects with unilateral amygdala damage (Adolphs et al., 2001), subjects with left temporal lobectomy performed slightly worse than brain-damaged controls, and subjects with right temporal lobectomy performed slightly worse yet. As a group, subjects with bilateral amygdala damage performed comparably to controls (Fig. 3 and Table 2), although we note the high score obtained by subject SM and the low score obtained by subject JM; these two subjects were also the youngest (32 years) and oldest (68 years), respectively. The performances in recognizing emotions from scenes including faces, across all stimuli or across only stimuli showing fear or sadness did not achieve statistically significant differences when comparing brain-damaged controls, subjects with unilateral amygdala damage (L and R combined), and subjects with bilateral amygdala damage (all P-values were non-significant, Mann–Whitney U-tests). However, subjects with bilateral amygdala damage did have significantly lower accuracy scores than brain-damaged controls in regard to scenes depicting anger (U=18.5, P<0.05, one-tailed uncorrected Mann–Whitney U-tests). Recognizing emotions from scenes: (a) mean performances (bars indicate S.E.M.) ... Fig. 3. Recognizing emotions from scenes: (a) mean performances (bars indicate S.E.M.) across all 16 stimuli when shown with faces; (b) mean performances for stimuli with faces erased. Bars (from left to right): brain-damaged controls (dark gray); left unilateral amygdala (left slanting stripes); right unilateral amygdala (right slanting stripes); subjects SM, RH, SZ and JM with bilateral amygdala damage (black). Figure options Table 2. Accuracy scores for scenes with faces given by subjects with bilateral amygdala damage and brain-damaged controls (BDC) SM RH SZ JM BDC Chance Total 0.83 0.63 0.56 0.39 0.72 0.22 Afraid 0.67 0.77 0.41 0.29 0.72 0.19 Angry 0.93 0.45 0.43 0.17 0.76 0.27 Sad 0.93 0.36 0.76 0.36 0.68 0.18 Happy 1.00 1.00 1.00 0.70 1.00 0.14 Surprised 0.46 0.64 0.67 0.64 0.60 0.25 Neutral 1.00 0.74 0.19 1.00 0.33 0.37 Chance: chance performance. Means are shown for BDC. Table options 3.2. Matching emotions to scenes without faces Our primary interest in this study, however, was to compare performances given to the same stimuli when they contained faces, and when the faces were erased. All subject groups showed the same trend: accuracy in recognizing emotions was compromised when faces had been erased from the stimuli, as one would expect (Fig. 3, right). However, a visual inspection of Fig. 3 suggests that subjects with bilateral amygdala damage do not show the same magnitude of this effect as do the other subject groups. When plotting the data only for scenes that signal anger, we found a surprising effect: whereas all other subject groups found these stimuli more difficult to recognize when faces had been erased, subjects with bilateral amygdala damage in fact showed superior accuracy for the scenes in which faces had been erased than for those in which faces were present (Fig. 4). Recognizing anger from scenes: (a) for stimuli with faces; (b) for stimuli with ... Fig. 4. Recognizing anger from scenes: (a) for stimuli with faces; (b) for stimuli with faces erased. Legend as in Fig. 3. Figure options To examine these findings in more detail, we calculated for each subject and each stimulus a difference score, the performance when the face was present compared to the performance when the face was erased. These difference scores are given for each emotion category in Table 3 and summarized in Fig. 5. For fear, sadness, and especially anger, subjects with bilateral amygdala damage benefited less when the face was included than did any other subject group. The highly unusual pattern seen for anger was present to a lesser extent also in the subjects with unilateral amygdala damage. Table 3. Difference scores (accuracy with faces minus accuracy without faces) for each emotion category given by the subject groups BDC Left Right Bilateral Total 0.16 0.13 0.13 0.06 Afraid 0.25 0.27 0.25 0.13 Angry 0.13 −0.03 −0.05 −0.22 Sad 0.09 0.10 0.12 0.06 Happy 0.18 0.10 0.08 0.13 Surprised 0.11 0.11 0.16 0.25 Neutral 0.00 0.07 0.26 0.18 BDC: brain-damaged controls; left: unilateral left amygdala damage; right: unilateral right amygdala damage; bilateral: bilateral amygdala damage (means are given). Table options Performances differences when recognizing emotion from scenes with faces ... Fig. 5. Performances differences when recognizing emotion from scenes with faces compared to scenes without faces, shown for all stimuli (left) and for anger only (right). Legend as in Fig. 3. Figure options For scenes showing positive emotions (happiness and surprise), all subject groups showed the largest proportion of trials in which they performed more accurately when shown scenes with faces than without faces. For scenes showing negative emotions (fear, anger, and sadness), subjects with bilateral amygdala damage showed precisely the opposite pattern, performing better without faces than with faces on the majority of trials. This abnormal pattern was most extreme in the case of scenes showing anger, where it is shown also to a lesser extent in subjects with unilateral amygdala damage (Fig. 6). Proportion of trials in which subjects were more accurate when shown scenes ... Fig. 6. Proportion of trials in which subjects were more accurate when shown scenes without faces than scenes with faces, for positive emotions (happy and surprise; left), negative emotions (fear, anger, and sadness; middle), and anger (right). Proportions were calculated on the basis of the total number of trials (subjects with bilateral amygdala who participated in multiple replications of the task thus contributed multiple data points for each stimulus). We here also show data from the normal controls (white bars), since we can calculate whether or not they performed better or worse, even though we cannot strictly use their absolute accuracy scores. Figure options We examined the mean performances given to all negatively valenced stimuli, both with and without faces. We found a significant difference among brain-damaged groups (F(2,46)=5.1, P<0.01) due to a significant pairwise difference only between brain-damaged controls and subjects with bilateral amygdala damage (P<0.01, post-hoc Scheffe test). This finding held up with a 3×3 group by negative emotion ANOVA: there was a significant effect of negative emotion category (F(2,138)=10.5, P<0.0001), a significant effect of subject group (F(2,138)=3.64, P<0.05), and no significant interaction. Post-hoc Scheffe tests again showed a significant pairwise difference only between brain-damaged controls and subjects with bilateral amygdala damage (P<0.05). When examining the proportion of subjects who performed better on scenes with faces erased, while there were no significant differences in proportions across the mean performance for all stimuli (χ2(2)=4.2, P>0.1), there were highly significant differences when examining performances for angry scenes (χ2(2)=19.1, P<0.0001). The groups with unilateral amygdala damage and those with bilateral amygdala damage showed a much higher proportion of subjects performing more accurately on angry scenes with faces erased than did brain-damaged controls (Fisher’s exact tests: P=0.0002 and 0.0023, respectively). 3.3. Recognizing anger When we examined the responses given to individual anger scenes, we found that subjects with amygdala damage show such an unusual pattern in large part because they give highly incorrect scores (obtaining an accuracy score of 0) for certain scenes containing angry facial expressions, but provide the correct answer (obtaining an accuracy score of 1) when the faces have been erased. In several cases, subjects with bilateral amygdala damage erroneously labeled scenes with angry faces as “happy”, and three out of the four subjects made this exact mistake on several occasions, whereas no subject in any of the other groups ever made this mistake. In several cases, the particular anger stimuli that were mistaken for happy stimuli showed facial expressions with an open mouth and bared teeth. We were able to compare the data from the present task with those obtained from recognition of angry facial expressions shown in isolation (from the “Pictures of facial affect”). These data, previously published for SM, JM and RH (Adolphs, 1999, Adolphs et al., 1994 and Adolphs et al., 1999), and new for SZ, show that all four subjects are impaired in their ability to recognize anger from facial expressions. When asked to rate the intensity of anger shown in angry faces, and compared to a group of 17 normal controls (Adolphs et al., 1999), the 4 subjects with bilateral amygdala damage gave intensity ratings that were below the normal mean intensity rating. Their Z-scores were as follows: SM, from −0.8 to −6.0 (three experiments); RH, −4.3; SZ, −3.9; JM, −5.5. 3.4. Effects of presentation order and of extent of amygdala damage There were no order effects in the subjects with bilateral amygdala damage, an issue we could investigate in the three subjects who were so densely amnesic that they did not remember having seen the stimuli on a prior occasion. Across three replications of the experiment, two of which were in the same order as given to other subjects (scenes without faces shown first) and one of which was in the reverse order (scenes with faces shown first), there were no significant differences in accuracy scores for scenes showing negative emotions (all P-values were non-significant; uncorrected Mann–Whitney U-tests between pairs of testing sessions). We also investigated if there might be a correlation between the extent of unilateral amygdala damage in the unilateral amygdala subjects, and their difference score in recognizing anger scenes. We found no significant correlation (Spearman’s ρ=0.25, non-significant).