Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits

Journal name:
Nature Neuroscience
Volume:
13,
Pages:
419–421
Year published:
DOI:
doi:10.1038/nn.2510
Received
Accepted
Published online

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.

At a glance

Figures

  1. Impulsive-antisocial traits predict nucleus accumbens DA release.
    Figure 1: Impulsive-antisocial traits predict nucleus accumbens DA release.

    (a) Statistical parametric map (SPM) showing that PPI-IA factor scores selectively predicted increased amphetamine-induced DA release in bilateral NAcc (left NAcc: −16, 10, −10, pfalse discovery rate = 0.003, z = 3.74, cluster size (k) = 56; right NAcc: 16, 18, −6; pfalse discovery rate = 0.002, z = 4.21, k = 44). All coordinates reference the coordinate system of the Montreal Neurological Institute. SPM thresholded at P < 0.05 (uncorrected) for visualization purposes. Color bar indicates t statistic value. (b,c) Scatter plot depicting the relationship between PPI-IA factor scores and amphetamine-induced DA release in left (b) and right (c) NAcc. DA release values were extracted from clusters defined by a pFDR < 0.05 threshold.

  2. Impulsive-antisocial factor scores are selectively associated with NAcc BOLD signal during monetary reward anticipation.
    Figure 2: Impulsive-antisocial factor scores are selectively associated with NAcc BOLD signal during monetary reward anticipation.

    (a) Image depicts the Harvard-Oxford nucleus accumbens anatomical ROI from which BOLD signal estimates were obtained. (b) Scatter plot depicts the relationship between PPI-IA factor scores and reward anticipation–related BOLD signal in the right NAcc.

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Author information

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

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.

Competing financial interests

The authors declare no competing financial interests.

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    Supplementary Figures 1–8, Supplementary Data, Supplementary Discussion and Supplementary Methods

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