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T He Human Amygdala and the Emotional Evaluation of Sensory Stimuli David H

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T He Human Amygdala and the Emotional Evaluation of Sensory Stimuli David H Brain Research Reviews 41 (2003) 88–123 www.elsevier.com/locate/brainresrev Review T he human amygdala and the emotional evaluation of sensory stimuli David H. Zald* Department of Psychology, Vanderbilt University, 301 Wilson Hall, 111 21 st Ave. S., Nashville, TN 37240-0009, USA Accepted 8 October 2002 Abstract A wealth of animal data implicates the amygdala in aspects of emotional processing. In recent years, functional neuroimaging and neuropsychological studies have begun to refine our understanding of the functions of the amygdala in humans. This literature offers insights into the types of stimuli that engage the amygdala and the functional consequences that result from this engagement. Specific conclusions and hypotheses include: (1) the amygdala activates during exposure to aversive stimuli from multiple sensory modalities; (2) the amygdala responds to positively valenced stimuli, but these responses are less consistent than those induced by aversive stimuli; (3) amygdala responses are modulated by the arousal level, hedonic strength or current motivational value of stimuli; (4) amygdala responses are subject to rapid habituation; (5) the temporal characteristics of amygdala responses vary across stimulus categories and subject populations; (6) emotionally valenced stimuli need not reach conscious awareness to engage amygdala processing; (7) conscious hedonic appraisals do not require amygdala activation; (8) activation of the amygdala is associated with modulation of motor readiness, autonomic functions, and cognitive processes including attention and memory; (9) amygdala activations do not conform to traditional models of the lateralization of emotion; and (10) the extent and laterality of amygdala activations are related to factors including psychiatric status, gender and personality. The strengths and weakness of these hypotheses and conclusions are discussed with reference to the animal literature. 2002 Elsevier Science B.V. All rights reserved. Theme: Neural basis of behavior Topic: Motivation and emotion Keywords: Emotion; Face; fMRI; Laterality; Lesion; PET Contents 1 . Introduction ............................................................................................................................................................................................ 89 2 . Methodological issues.............................................................................................................................................................................. 89 2 .1. Neuroimaging ................................................................................................................................................................................. 89 2 .2. Lesion studies ................................................................................................................................................................................. 91 3 . Multimodal responses to aversive stimuli .................................................................................................................................................. 92 4 . Positively valenced stimuli and the importance of arousal and motivation.................................................................................................... 95 4 .1. Arousal .......................................................................................................................................................................................... 95 4 .2. Sexual arousal................................................................................................................................................................................. 95 4 .3. Appetitive motivation and drug craving ............................................................................................................................................ 97 4 .4. Perceptual intensity ......................................................................................................................................................................... 98 4 .5. The amygdala sometimes shows decreased activity in response to highly positive emotional stimuli ..................................................... 98 5 . Facial expressions.................................................................................................................................................................................... 99 6 . Semantic and nonverbal auditory processing.............................................................................................................................................. 102 7 . Contrasting the effects of positively and negatively valenced stimuli ........................................................................................................... 103 8 . Habituation, temporal characteristics and novelty....................................................................................................................................... 104 *Tel.: 11-615-343-6076; fax: 11-615-343-8449. E-mail address: [email protected] (D.H. Zald). 0165-0173/02/$ – see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S0165-0173(02)00248-5 D.H. Zald / Brain Research Reviews 41 (2003) 88–123 89 9 . Subliminal processing .............................................................................................................................................................................. 106 1 0. Laterality issues..................................................................................................................................................................................... 107 1 0.1. Models of emotion lateralization..................................................................................................................................................... 107 1 0.2. Other hypotheses regarding lateralization ........................................................................................................................................ 108 1 1. The functional consequences of amygdala engagement............................................................................................................................. 109 1 1.1. Memory enhancement.................................................................................................................................................................... 109 1 1.2. Conditioning ................................................................................................................................................................................. 109 1 1.3. Attention modulation ..................................................................................................................................................................... 109 1 1.4. Startle, hormonal and autonomic modulation ................................................................................................................................... 110 1 1.5. The relationship between amygdala engagement and the modulation of cognitive, motoric, and endocrine responses ............................ 111 1 2. Task demands: the effects of explicit emotional evaluation on amygdala activity........................................................................................ 111 1 3. Restricted influence of the amygdala on conscious emotional evaluation and subjective emotional experience .............................................. 112 1 4. Group and individual differences in amygdala responsiveness................................................................................................................... 113 1 4.1. Gender differences ........................................................................................................................................................................ 113 1 4.2. Handedness................................................................................................................................................................................... 113 1 4.3. Psychopathology and individual differences .................................................................................................................................... 113 1 5. Conclusions and future directions............................................................................................................................................................ 114 Acknowledgements ...................................................................................................................................................................................... 115 References................................................................................................................................................................................................... 115 1 . Introduction refining our theories of amygdala functioning. This article provides an overview of this emerging literature and Neurobehavioral theorists have frequently argued that outlines several of the unique insights provided by this the amygdala plays a central role in the emotional process- research. ing of sensory stimuli. Electrophysiological, neurophar- macological, and lesion studies in animals, have all provided support for the involvement of the amygdala in 2 . Methodological issues both the evaluation and response to emotionally salient stimuli. However, there exists a strong need for human 2 .1. Neuroimaging data. The relative distribution
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