Reduced prefrontal connectivity in psychopathy

Abstract

Linking psychopathy to a specific brain abnormality could have significant clinical, legal, and scientific implications. Theories on the neurobiological basis of the disorder typically propose dysfunction in a circuit involving ventromedial prefrontal cortex (vmPFC). However, to date there is limited brain imaging data to directly test whether psychopathy may indeed be associated with any structural or functional abnormality within this brain area. In this study, we employ two complementary imaging techniques to assess the structural and functional connectivity of vmPFC in psychopathic and non-psychopathic criminals. Using diffusion tensor imaging, we show that psychopathy is associated with reduced structural integrity in the right uncinate fasciculus, the primary white matter connection between vmPFC and anterior temporal lobe. Using functional magnetic resonance imaging, we show that psychopathy is associated with reduced functional connectivity between vmPFC and amygdala as well as between vmPFC and medial parietal cortex. Together, these data converge to implicate diminished vmPFC connectivity as a characteristic neurobiological feature of psychopathy.

Figure 1.

DTI results: reduced white matter integrity is specific to the right UF in psychopaths. a, The UF ROI (circled in red) in serial axial slices and a single coronal slice. b, The UF ROI (red) superimposed on an entire UF tract, as computed with tractography (see Materials and Methods for additional details). c–e, Bar plots of mean scaled FA values in three comparison tracts, in each hemisphere: ILF/IFOF (c), SLF (d), and SFOF (e). f, Bar plots of mean scaled FA values in the UF. Psychopaths exhibited significantly lower scaled FA values only in right UF. Error bars indicate SEM. *p < 0.05.

Figure 2.

Functional connectivity between the right amygdala and anterior vmPFC is reduced in psychopaths. a, Group differences in connectivity were assessed in the vmPFC mask (red) for correlation coefficients computed using the mean time series extracted from the hand drawn right amygdala seed (blue). b, Mean right amygdala–vmPFC connectivity maps for non-psychopaths and psychopaths are shown separately on the group mean anatomical image, thresholded at a cluster corrected p < 0.05. Scale bars depict the uncorrected t statistic. Both groups exhibit significant resting connectivity between right amygdala and regions of vmPFC. The group difference map indicates an area in anterior vmPFC where non-psychopaths have significantly greater connectivity than psychopaths (x = −3, y = −66, z = −10, cluster size = 14 voxels). c, A three-dimensional rendering of the group mean anatomical image shows the location of the amygdala seed (blue) and significant vmPFC cluster (red) in relation to the UF (green). d, The bar plot depicts the significant group difference in connectivity estimates (Fisher z-transformed correlation coefficients) within the vmPFC cluster. Error bars indicate SEM. Filled circles represent values from individual subjects.

Figure 3.

Functional connectivity between medial parietal cortex and vmPFC is reduced in psychopaths. a, Mean precuneus/PCC–vmPFC connectivity maps are depicted separately for non-psychopaths and psychopaths on the group mean anatomical image, thresholded at a cluster corrected p < 0.05. Scale bars indicate the uncorrected t statistic. Both groups exhibit significant resting connectivity between right precuneus/PCC and regions of vmPFC. The group difference map indicates two separate clusters within vmPFC where non-psychopaths have significantly greater connectivity with the precuneus/PCC seed than psychopaths (vmPFC: x = −12, y = −51, z = −12, cluster size = 27 voxels; rACC: x = −9, y = −39, z = +6, cluster size = 15 voxels). b, Group differences in connectivity were assessed in the vmPFC mask (red) for correlation coefficients computed using the mean time series extracted from the PCC seed (blue; x = −5, y = +49, z = +40). c, The bar plots depict group differences in connectivity estimates (Fisher z-transformed correlation coefficients) within each significant cluster. Error bars indicate SEM. Filled circles represent values from individual subjects.

Figure 4.

Analysis of DTI and rest-fMRI findings with respect to psychopathy subtype. a, Depiction of each significant finding in the main between-group analyses (psychopaths vs non-psychopaths). b, For right UF FA values, among non-psychopaths, the low- and high-anxious subgroups significantly differ (p = 0.046); there is no such difference among psychopaths. c, For the cluster identified in the right amygdala–vmPFC connectivity analysis, there is a significant interaction between psychopathy and anxiety (p = 0.005), indicating that connectivity is differentially modulated by anxiety subgroup in psychopaths and non-psychopaths. d, e, There are no significant interactions between psychopathy and anxiety for medial parietal–vmPFC connectivity. Error bars indicate SEM. Asterisks indicate significant differences between anxiety subtypes.