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Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits

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Abstract

Psychopathy is a personality disorder that is strongly linked to criminal behavior. Using [18F]fallypride positron emission tomography and blood oxygen level–dependent functional magnetic resonance imaging, we found that impulsive-antisocial psychopathic traits selectively predicted nucleus accumbens dopamine release and reward anticipation-related neural activity in response to pharmacological and monetary reinforcers, respectively. These findings suggest that neurochemical and neurophysiological hyper-reactivity of the dopaminergic reward system may comprise a neural substrate for impulsive-antisocial behavior and substance abuse in psychopathy.

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Figure 1: Impulsive-antisocial traits predict nucleus accumbens DA release.
Figure 2: Impulsive-antisocial factor scores are selectively associated with NAcc BOLD signal during monetary reward anticipation.

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Acknowledgements

We thank B. Knutson for kindly making the monetary incentive delay task available and C. Weiner and M. McHugo for assistance with fMRI scanning and data analysis. This research was funded by the National Institute on Drug Abuse (R01DA019670-04).

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Authors and Affiliations

  1. Department of Psychology, Vanderbilt University, Nashville, Tennessee, USA

    Joshua W Buckholtz, Michael T Treadway, Ronald L Cowan, Stephen D Benning, Ashley N Schwartzman, Evan S Shelby & David H Zald

  2. Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee, USA

    Joshua W Buckholtz

  3. Department of Psychiatry, Vanderbilt University, Nashville, Tennessee, USA

    Ronald L Cowan, Neil D Woodward & David H Zald

  4. Department of Radiology, Vanderbilt University, Nashville, Tennessee, USA

    Rui Li, M Sib Ansari, Ronald M Baldwin, Clarence E Smith & Robert M Kessler

  5. Department of Psychology and Human Development, Vanderbilt University, Nashville, Tennessee, USA

    David Cole

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  1. Joshua W Buckholtz
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  2. Michael T Treadway
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  3. Ronald L Cowan
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  4. Neil D Woodward
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  5. Stephen D Benning
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  6. Rui Li
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  7. M Sib Ansari
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  8. Ronald M Baldwin
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  9. Ashley N Schwartzman
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  10. Evan S Shelby
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  12. David Cole
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Contributions

J.W.B., R.M.K. and D.H.Z. designed the study. E.S.S. and A.N.S. recruited participants into the study and collected PET and personality data. J.W.B. collected fMRI data with assistance from E.S.S., and A.N.S., R.L., N.D.W. and R.M.K. performed single-subject PET data analysis and quality control. J.W.B. performed group level PET data analysis with assistance from M.T.T. J.W.B. analyzed fMRI data at all stages. M.S.A. and R.M.B. synthesized radio-labeled fallypride for PET scanning. S.D.B. provided conceptual advice, statistical support and supplementary analyses for the PPI data. R.L.C. oversaw all medical aspects of the protocol. C.E.S. and R.M.K. provided medical support for PET scanning. D.C. provided conceptual support and statistical advice for the study. J.W.B., M.T.T. and D.H.Z. wrote the manuscript with assistance from R.L.C.

Corresponding author

Correspondence to Joshua W Buckholtz.

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Competing interests

The authors declare no competing financial interests.

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Supplementary Text and Figures

Supplementary Figures 1–8, Supplementary Data, Supplementary Discussion and Supplementary Methods (PDF 879 kb)

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Buckholtz, J., Treadway, M., Cowan, R. et al. Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits. Nat Neurosci 13, 419–421 (2010). https://doi.org/10.1038/nn.2510

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