Disrupted Prefrontal Regulation of Striatal Subjective Value Signals in Psychopathy

Jay G Hosking; Erik K Kastman; Hayley M Dorfman; Gregory R Samanez-Larkin; Arielle Baskin-Sommers; Kent A Kiehl; Joseph P Newman; Joshua W Buckholtz

doi:10.1016/j.neuron.2017.06.030

Disrupted Prefrontal Regulation of Striatal Subjective Value Signals in Psychopathy

Neuron. 2017 Jul 5;95(1):221-231.e4. doi: 10.1016/j.neuron.2017.06.030.

Authors

Jay G Hosking¹, Erik K Kastman², Hayley M Dorfman², Gregory R Samanez-Larkin³, Arielle Baskin-Sommers⁴, Kent A Kiehl⁵, Joseph P Newman⁶, Joshua W Buckholtz⁷

Affiliations

¹ Department of Psychology, Harvard University, 52 Oxford St., Cambridge, MA 02138, USA. Electronic address: jhosking@fas.harvard.edu.
² Department of Psychology, Harvard University, 52 Oxford St., Cambridge, MA 02138, USA.
³ Department of Psychology and Neuroscience, Duke University, 417 Chapel Dr., Durham, NC 27708, USA.
⁴ Department of Psychology, Yale University, 2 Hillhouse Ave., New Haven, CT 06520, USA.
⁵ MIND Institute, 1101 Yale Blvd NE, Albuquerque, NM 87106, USA.
⁶ Department of Psychology, University of Wisconsin-Madison, 1202 W Johnson St., Madison, WI 53706, USA.
⁷ Department of Psychology, Harvard University, 52 Oxford St., Cambridge, MA 02138, USA; Center for Brain Science, Harvard University, 52 Oxford St., Cambridge, MA 02138, USA; Department of Psychiatry, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02144, USA. Electronic address: joshua_buckholtz@harvard.edu.

Abstract

Psychopathy is a personality disorder with strong links to criminal behavior. While research on psychopathy has focused largely on socio-affective dysfunction, recent data suggest that aberrant decision making may also play an important role. Yet, the circuit-level mechanisms underlying maladaptive decision making in psychopathy remain unclear. Here, we used a multi-modality functional imaging approach to identify these mechanisms in a population of adult male incarcerated offenders. Psychopathy was associated with stronger subjective value-related activity within the nucleus accumbens (NAcc) during inter-temporal choice and with weaker intrinsic functional connectivity between NAcc and ventromedial prefrontal cortex (vmPFC). NAcc-vmPFC connectivity strength was negatively correlated with NAcc subjective value-related activity; however, this putative regulatory pattern was abolished as psychopathy severity increased. Finally, weaker cortico-striatal regulation predicted more frequent criminal convictions. These data suggest that cortico-striatal circuit dysregulation drives maladaptive decision making in psychopathy, supporting the notion that reward system dysfunction comprises an important neurobiological risk factor.

Keywords: antisocial; cortico-striatal; delay discounting; functional connectivity; psychopathy; reward; self-control; striatum; value-based decision making; ventromedial prefrontal cortex.

MeSH terms

Adult
Antisocial Personality Disorder / physiopathology*
Antisocial Personality Disorder / psychology
Criminals*
Decision Making
Functional Neuroimaging
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Neural Pathways / diagnostic imaging
Neural Pathways / physiopathology
Nucleus Accumbens / diagnostic imaging
Nucleus Accumbens / physiopathology*
Prefrontal Cortex / diagnostic imaging
Prefrontal Cortex / physiopathology*
Prisoners*
Severity of Illness Index
Ventral Striatum / diagnostic imaging
Ventral Striatum / physiopathology
Young Adult

Abstract

MeSH terms

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