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Science 28 July 2000:
Vol. 289. no. 5479, pp. 591 - 594
DOI: 10.1126/science.289.5479.591
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Review

Dysfunction in the Neural Circuitry of Emotion Regulation--A Possible Prelude to Violence

Richard J. Davidson,* Katherine M. Putnam, Christine L. Larson

Emotion is normally regulated in the human brain by a complex circuit consisting of the orbital frontal cortex, amygdala, anterior cingulate cortex, and several other interconnected regions. There are both genetic and environmental contributions to the structure and function of this circuitry. We posit that impulsive aggression and violence arise as a consequence of faulty emotion regulation. Indeed, the prefrontal cortex receives a major serotonergic projection, which is dysfunctional in individuals who show impulsive violence. Individuals vulnerable to faulty regulation of negative emotion are at risk for violence and aggression. Research on the neural circuitry of emotion regulation suggests new avenues of intervention for such at-risk populations.

Laboratory for Affective Neuroscience and W. M. Keck Laboratory for Functional Brain Imaging and Behavior, University of Wisconsin-Madison, Madison, WI 53706, USA.
*   To whom correspondence should be addressed. E-mail: rjdavids{at}facstaff.wisc.edu.

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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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