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Articles, Behavioral/Cognitive

Parsing the Behavioral and Brain Mechanisms of Third-Party Punishment

Matthew R. Ginther, Richard J. Bonnie, Morris B. Hoffman, Francis X. Shen, Kenneth W. Simons, Owen D. Jones and René Marois
Journal of Neuroscience 7 September 2016, 36 (36) 9420-9434; DOI: https://doi.org/10.1523/JNEUROSCI.4499-15.2016
Matthew R. Ginther
1Neuroscience Graduate Program, Vanderbilt University, Nashville, Tennessee 37203,
2Vanderbilt Law School, Nashville, Tennessee 37203,
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Richard J. Bonnie
3Institute of Law, Psychiatry and Public Policy, University of Virginia School of Law, Charlottesville, Virginia 22903,
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Morris B. Hoffman
4District Judge, Second Judicial District (Denver), State of Colorado, Denver, Colorado 80202,
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Francis X. Shen
5Department of Law, University of Minnesota, Minneapolis, Minnesota 55455,
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Kenneth W. Simons
6Department of Law, University of California, Irvine School of Law, Irvine, California 92697,
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Owen D. Jones
2Vanderbilt Law School, Nashville, Tennessee 37203,
7Departments of Law and Biological Sciences, Vanderbilt University, Nashville, Tennessee 37203,
8Director, MacArthur Foundation Research Network on Law and Neuroscience,
9Center for Integrative and Cognitive Neuroscience, and
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René Marois
9Center for Integrative and Cognitive Neuroscience, and
10Department of Psychology, Vanderbilt University, Nashville, Tennessee 37240
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Abstract

The evolved capacity for third-party punishment is considered crucial to the emergence and maintenance of elaborate human social organization and is central to the modern provision of fairness and justice within society. Although it is well established that the mental state of the offender and the severity of the harm he caused are the two primary predictors of punishment decisions, the precise cognitive and brain mechanisms by which these distinct components are evaluated and integrated into a punishment decision are poorly understood. Using fMRI, here we implement a novel experimental design to functionally dissociate the mechanisms underlying evaluation, integration, and decision that were conflated in previous studies of third-party punishment. Behaviorally, the punishment decision is primarily defined by a superadditive interaction between harm and mental state, with subjects weighing the interaction factor more than the single factors of harm and mental state. On a neural level, evaluation of harms engaged brain areas associated with affective and somatosensory processing, whereas mental state evaluation primarily recruited circuitry involved in mentalization. Harm and mental state evaluations are integrated in medial prefrontal and posterior cingulate structures, with the amygdala acting as a pivotal hub of the interaction between harm and mental state. This integrated information is used by the right dorsolateral prefrontal cortex at the time of the decision to assign an appropriate punishment through a distributed coding system. Together, these findings provide a blueprint of the brain mechanisms by which neutral third parties render punishment decisions.

SIGNIFICANCE STATEMENT Punishment undergirds large-scale cooperation and helps dispense criminal justice. Yet it is currently unknown precisely how people assess the mental states of offenders, evaluate the harms they caused, and integrate those two components into a single punishment decision. Using a new design, we isolated these three processes, identifying the distinct brain systems and activities that enable each. Additional findings suggest that the amygdala plays a crucial role in mediating the interaction of mental state and harm information, whereas the dorsolateral prefrontal cortex plays a crucial, final-stage role, both in integrating mental state and harm information and in selecting a suitable punishment amount. These findings deepen our understanding of how punishment decisions are made, which may someday help to improve them.

  • decision-making
  • fMRI
  • harm
  • law
  • mental state
  • punishment

This article is freely available online through the J Neurosci Author Open Choice option.

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The Journal of Neuroscience: 36 (36)
Journal of Neuroscience
Vol. 36, Issue 36
7 Sep 2016
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Parsing the Behavioral and Brain Mechanisms of Third-Party Punishment
Matthew R. Ginther, Richard J. Bonnie, Morris B. Hoffman, Francis X. Shen, Kenneth W. Simons, Owen D. Jones, René Marois
Journal of Neuroscience 7 September 2016, 36 (36) 9420-9434; DOI: 10.1523/JNEUROSCI.4499-15.2016

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Parsing the Behavioral and Brain Mechanisms of Third-Party Punishment
Matthew R. Ginther, Richard J. Bonnie, Morris B. Hoffman, Francis X. Shen, Kenneth W. Simons, Owen D. Jones, René Marois
Journal of Neuroscience 7 September 2016, 36 (36) 9420-9434; DOI: 10.1523/JNEUROSCI.4499-15.2016
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Keywords

  • decision-making
  • fMRI
  • harm
  • law
  • mental state
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