Recognizing Facial Emotion C: 1.0 ~ ~!GT

en 'Oil Recognizing facial emotion C: 1.0 ~ ~!GT ... 0 . EP ~ EP O ij G m EP GT 84 ~t GT SIR-The amygdala has been implicated in and G.T., aged 73 and 59 years, respective E 0.8 0 0 It ~ GT 8 EP emotion and emotional memory in humans ly), with complete bilateral lesions of the C: i EP 12 3 EP O and experimental animals • . Some of us amygdala and additional temporal lobe B o0 "' GTOI en 0.6 'Oil have reported impaired recognition of structures (Fig. 1). Despite this, they C: emotion in facial expressions ( especially appear unimpaired in recognizing facial -~ 0.4 t fear) in a 30-year-old woman (S.M.) with a expressions of emotion, including fear. E.P 0 -C: 0 nearly complete bilateral lesion of the and G.T. are profoundly amnesic but have :;:; amygdala due to congenital Urbach IQ scores in the normal range. ro 0 .2 ~ Wiethe disease. This suggested that the E.P. and G.T. were tested twice, once 0 (.) .. 0 amygdala may be essential not only for using the exact materials and procedure C: Happy Surpnsed Afraid Angry Disgusted Sad emotional learning, but also for recog reported by Adolphs et al. 3 (Fig. 2), and "'brain-damaged controls (circles; n= 12), S.M.'s ratings (triangles show results for patients performed similarly to four age 4 experiments), E.P.'s ratings (EP; 1 expt), and and education-matched controls in every G.T.'s ratings (GT; 1 expt). Data for the brain• respect ( correlations between groups damaged controls and S.M. are from Adolphs et >0.70 for each of the six emotions). For a/. 3 • Data for E.P. and G.T. are from an experi• faces consistent with the emotion being ment that replicated the procedures used there• rated, the patients obtained an average in. Recognition of facial expression of human rating of 4.6 ( 4.8 for fear) on a 0-5 scale; emotion was tested by presenting on a screen and one at a time 6 different expressions of control rating was 4.3 ( 4.3 for fear). facial emotion (each displayed by 6 different There are two possibilities consistent faces). Subjects rated each face with respect to with these data. One possibility is that 9 adjectives (the 6 emotions shown in the figure, bilateral damage to the amygdala together as well as awake, sleepy or interested). with damage outside the amygdala is required to impair the recognition of absence of damage early in life, recog facial emotion. Intracranial lesions result nition of facial emotion in adults does not ing from Urbach-Wiethe disease can have an absolute dependence on the extend beyond the amygdala to include amygdala. These data and conclusions other structures5·6• In addition to her are fully compatible with an important amygdala lesion, S.M. has minimal dam role for the amygdala in the experience age to the entorhinal cortex2 on the left and expression of emotion. Tasks that side. Moreover, postmortem histopath assess the recognition of fear in facial ological analysis may reveal damage not expressions may not require the actual detected by current neuroimaging tech experience of fear. niques. Damage to the basal ganglia is Stephan B. Hamann, Lisa Stefanacci reported to impair the recognition of Department of Psychiatry, facial emotion 7, although it is unclear that University of California, such impairment is similar to that of S.M. San Diego, California 92093, USA A more likely possibility is that amyg Larry R. Squire dala lesions impair the recognition of Departments of Psychiatry emotion in facial expressions only if these and Neurosciences, lesions occur early in development, rather University of California, San Diego, California 92093, USA and FIG. 1 a, Coronal Ti-weighted magnetic res• than in adulthood. The Urbach- Wiethe onance image of patient E.P. showing extensive disease that led to S.M.'s amygdaloid VA Medical Center, bilateral damage to the amygdaloid complex lesions is congenital, whereas E.P. and G.T. San Diego, California 92161, USA (arrows). The damage extends rostrally to the sustained their lesions after the age of 50 Ralph Adolphs, Daniel Tranel temporal pole and caudally to include the years. D.R., a 51-year-old woman who is Hanna Damaslo, Antonio Damasio hippocampal formation. There is also severe also deficient in recognizing facial Department of Neurology, atrophy of the entorhinal, perirhinal and para• emotion8, sustained partial bilateral lesions University of Iowa, College of Medicine, hippocampal cortices. b, Coronal Ti-weighted Iowa City, Iowa 52242, USA magnetic resonance image of patient G.T. at a to the amygdala and to the right basal similar rostrocaudal level, showing severe ganglia in adulthood. However, D.R. has a 1. LeDoux, J. Behav. Brain Res. 58, 69- 79 (1993). 2. Bechara, A. et al. Science 269, 1115- 1118 (1995). bilateral temporal lobe damage (arrows). The history of epilepsy and a broader deficit 3 . Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. damage extends through the anterior 7.0 cm of than S.M. in processing emotions. Perhaps Nature 372, 669- 672 (1994). G.T.'s left temporal lobe and through the anter• a combination of factors, including a 4. Squire, L. & Knowlton, B. Proc. natn. Acad. Sci. U.S.A. ior 5.0 cm of his right temporal lobe. The lesion 92, 12470- 12474 (1995). congenital lesion, low full-scale IQ 5. Friedman, D., Mathews, R. & Swanepoel, P. S. Afr. med. bilaterally includes the amygdaloid complex, (S.M. = 86, D.R.= 87) and/or additional }. 65, 734-735 (1984). hippocampus, entorhinal, peri rhinal and para• 6. Newton, F., Rosenberg, R., Lampert, P. & O'Brien, J. hippocampal cortices as well as the inferior, brain damage, could determine how Neurology 21, 1205-1213 (1971). middle and superior temporal gyri , There is also readily other strategies are available for 7. Jacobs, D., Shuren, J., Bowers, D. & Heilman, K. Neurology 45, 1696--1702 (1995). bilateral damage in the insular cortex, medial recognizing facial emotion. 8. Young, A. . Hellawell. D .. van de Wal, C. & Johnson, M. and orbital frontal cortex, and cingulate gyrus. The present report suggests that in the Neuropsychologia (in the press) NATURE · VOL 379 · 8 FEBRUARY 1996 497