Lesion network localization of criminal behavior

R Ryan Darby, Andreas Horn, Fiery Cushman, Michael D Fox, R Ryan Darby, Andreas Horn, Fiery Cushman, Michael D Fox

Abstract

Following brain lesions, previously normal patients sometimes exhibit criminal behavior. Although rare, these cases can lend unique insight into the neurobiological substrate of criminality. Here we present a systematic mapping of lesions with known temporal association to criminal behavior, identifying 17 lesion cases. The lesion sites were spatially heterogeneous, including the medial prefrontal cortex, orbitofrontal cortex, and different locations within the bilateral temporal lobes. No single brain region was damaged in all cases. Because lesion-induced symptoms can come from sites connected to the lesion location and not just the lesion location itself, we also identified brain regions functionally connected to each lesion location. This technique, termed lesion network mapping, has recently identified regions involved in symptom generation across a variety of lesion-induced disorders. All lesions were functionally connected to the same network of brain regions. This criminality-associated connectivity pattern was unique compared with lesions causing four other neuropsychiatric syndromes. This network includes regions involved in morality, value-based decision making, and theory of mind, but not regions involved in cognitive control or empathy. Finally, we replicated our results in a separate cohort of 23 cases in which a temporal relationship between brain lesions and criminal behavior was implied but not definitive. Our results suggest that lesions in criminals occur in different brain locations but localize to a unique resting state network, providing insight into the neurobiology of criminal behavior.

Keywords: criminality; functional connectivity; lesion; morality; sociopathy.

Conflict of interest statement

The authors declare no conflict of interest.

Copyright © 2018 the Author(s). Published by PNAS.

Figures

Fig. 1.
Fig. 1.
Lesions temporally associated with criminal behavior. Lesions from 17 patients with acquired criminal behavior, manually traced onto a common brain atlas (MNI).
Fig. 2.
Fig. 2.
Lesion network mapping technique. (A) Lesions traced onto a standardized MNI brain template. (B) Brain regions functionally connected to each lesion location based on a large resting-state functional connectivity database. (C) Overlap in the functional connectivity maps from each lesion identifies brain regions functionally connected to the greatest number of lesion locations.
Fig. 3.
Fig. 3.
Lesions temporally associated with criminality are part of a unique connected brain network. (A) Regions functionally connected to 17 lesion locations temporally associated with criminal behavior. (B) Nonparametric voxel-wise lesion-symptom mapping results showing regions in which 17 lesions temporally associated with criminal behavior were significantly more connected (positive in red, negative in blue) compared with the connectivity of 63 lesions causing other syndromes.
Fig. 4.
Fig. 4.
Lesions temporally associated with criminality are functionally connected to morality regions. (A) Regions functionally connected to lesion locations temporally associated with criminal behavior (red) are similar to regions activated by moral decision-making tasks (green; overlap in yellow). (B and C) Lesion locations temporally associated with criminal behavior (gray) are functionally connected to regions activated by moral decision-making tasks identified in meta-analyses using Neurosynth (B) or ALE (C), unlike lesions causing other neurologic syndromes (control syndromes; black). **P < 0.0001.
Fig. 5.
Fig. 5.
Lesions temporally associated with criminality are functionally connected to some, but not all, subcomponents of moral decision making. Connectivity with lesion locations temporally associated with criminal behavior (red) is similar to that in regions activated by some but not other components of moral decision making (green; overlap in yellow). Quantitatively, lesion locations temporally associated with criminal behavior are functionally connected to regions activated by value-based decision making (A) and theory of mind tasks (B), but not with empathy (C) or cognitive control tasks (D). These results were specific to lesions temporally associated with criminal behavior (gray) compared with lesions causing other neurologic syndromes (control syndromes; black). **P < 0.0001.
Fig. 6.
Fig. 6.
Lesions temporally associated with criminality are connected in opposite directions to opponent networks involved in moral decision making. (A) Lesion locations are positively connected (red) with regions activated by decisions to avoid harm in personal moral dilemmas (green; overlap in yellow). (B) Lesion locations are negatively connected (blue) with regions activated by utilitarian decisions in impersonal moral dilemmas (green; overlap in yellow). Results are specific to lesions temporally associated with criminal behavior (gray) compared with lesions causing other neurologic syndromes (black). **P < 0.0001.
Fig. 7.
Fig. 7.
Replication in lesions of uncertain temporal association with criminal behavior. Lesions with a clear temporal association (original cohort) (A) and uncertain temporal association (replication cohort) (B) are connected to the same regions (lesion network overlap, Right; voxel-wise nonparametric comparison with control syndromes, Middle). Lesions in both cohorts were significantly connected to regions involved in morality compared with control lesions (Right). **P < 0.0001.

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