Rapid publicationAmygdala damage impairs emotion recognition from scenes only when they contain 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, 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, 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.
Section snippets
Participants
We compared performances given by 4 individuals with bilateral amygdala damage with 2 other brain-damaged groups: 23 subjects with unilateral amygdala damage, and 22 brain-damaged controls without amygdala damage. Performances were converted to accuracy scores on the basis of data from a reference group of 16 neurologically normal controls (see below). All brain-damaged participants were recruited from the Division of Cognitive Neuroscience’s Patient Registry, and had been extensively
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
Discussion
The present findings provide additional detail to the role of the amygdala in recognizing emotions from visual stimuli depicting people. We can make the following conclusions:
- (1)
Bilateral amygdala damage impairs recognition of negative emotions from facial expressions. This finding has been shown in prior publications already.
- (2)
Bilateral amygdala damage does not in general impair recognition of emotions from complex static visual stimuli, provided those stimuli contain cues in addition to facial
Acknowledgments
We thank Antonio Damasio for providing the original stimuli and encouraging this study, and Jeremy Nath, Matt Karafin, and Barbara Majewska for help in testing subjects. Supported by National Institute of Neurological Diseases and Stroke Program Project Grant P01 19632 and the James S. McDonnell Foundation.
References (34)
- et al.
Recognition of facial emotion in nine subjects with bilateral amygdala damage
Neuropsychologia
(1999) - et al.
Social perception from visual cues: Role of the STS region
Trends in Cognitive Science
(2000) - et al.
Face processing impairments after encephalitis: Amygdala damage and recognition of fear
Neuropsychologia
(1998) - et al.
Brainvox: An interactive, multi-modal visualization and analysis system for neuroanatomical imaging
NeuroImage
(1997) - et al.
Single neuron activity in human hippocampus and amygdala during recognition of faces and objects
Neuron
(1997) - et al.
The distributed human neural system for face perception
Trends in Cognitive Science
(2000) - et al.
Face and voice expression identification in patients with emotional and behavioral changes following ventral frontal lobe damage
Neuropsychologia
(1996) - et al.
Neurons in the amygdala of the monkey with responses selective for faces
Behavioral Brain Research
(1985) - et al.
Facial expression processing after amygdalotomy
Neuropsychologia
(1996) The human amygdala and emotion
The Neuroscientist
(1999)