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. 2021 Feb 1;42(2):329-344.
doi: 10.1002/hbm.25225. Epub 2020 Oct 16.

Dynamic neural circuit disruptions associated with antisocial behaviors

Weixiong Jiang  1   2 , Han Zhang  1 , Ling-Li Zeng  3 , Hui Shen  3 , Jian Qin  3 , Kim-Han Thung  1 , Pew-Thian Yap  1 , Huasheng Liu  4 , Dewen Hu  3 , Wei Wang  4 , Dinggang Shen  1   5
Affiliations

Dynamic neural circuit disruptions associated with antisocial behaviors

Weixiong Jiang et al. Hum Brain Mapp. .

Abstract

Antisocial behavior (ASB) is believed to have neural substrates; however, the association between ASB and functional brain networks remains unclear. The temporal variability of the functional connectivity (or dynamic FC) derived from resting-state functional MRI has been suggested as a useful metric for studying abnormal behaviors including ASB. This is the first study using low-frequency fluctuations of the dynamic FC to unravel potential system-level neural correlates with ASB. Specifically, we individually associated the dynamic FC patterns with the ASB scores (measured by Antisocial Process Screening Device) of the male offenders (age: 23.29 ± 3.36 years) based on machine learning. Results showed that the dynamic FCs were associated with individual ASB scores. Moreover, we found that it was mainly the inter-network dynamic FCs that were negatively associated with the ASB severity. Three major high-order cognitive functional networks and the sensorimotor network were found to be more associated with ASB. We further found that impaired behavior in the ASB subjects was mainly associated with decreased FC dynamics in these networks, which may explain why ASB subjects usually have impaired executive control and emotional processing functions. Our study shows that temporal variation of the FC could be a promising tool for ASB assessment, treatment, and prevention.

Keywords: antisocial behavior; brain network; cognitive control function; default mode network; dynamic functional connectivity; functional MRI; resting state.

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Conflict of interest statement

The authors declare no conflict of interest. Dinggang Shen was involved in this work but he is now in a full‐time position with a new affiliation (United Imaging Intelligence, a subsidiary of United Imaging Healthcare Co., Ltd.).

Figures

FIGURE 1
FIGURE 1
Association analysis of antisocial behavior (ASB) scores with dFC patterns. (a) Individual dynamic functional connections and their variability calculations; (b) Schematic of SVR association with nested leaveone‐out cross‐validation (LOOCV) which consisted of inner and outer layers. The inner LOOCV was used to optimize the predictive model by feature selection (p‐value from a predefined range .005–.05, with a step of .001), then the optimal model (the selected features with the optimized p‐value) was used to generate the result for the left‐out sample in an outer LOOCV
FIGURE 2
FIGURE 2
The brain‐behavior association between dFC patterns and ASB scores. (a) Scatter plot between the model‐generated and the observed ASB scores for the integrated model. (b) Scatter plot between the model‐generated and observed ASB scores for the dFC between CON and FPN. (c) Scatter plot between the model‐generated and observed ASB scores with the dFC between DMN and FPN
FIGURE 3
FIGURE 3
The dFC‐ALFF links that were consistently selected during ASB‐brain association, including (a) Functional connections with negative correlation with the antisocial behavior score, and (b) Functional connections with positive correlation with the antisocial behavior score. Curves in colors indicate intra‐network dFC links; gray curves indicate inter‐network dFC links. CereN, cerebellum; CON, cingulo‐opercular network; DMN, default mode network; FPN, fronto‐parietal network; OcN, occipital network; SMN, sensorimotor network
FIGURE 4
FIGURE 4
ROI‐level degree of associations with ASB scores. The size of each ROI was proportional to its ASB associative level (i.e., the degree of contributions to ASB‐brain association). For the definition of the ASB associative level, see main text. CereN, cerebellum; CON, cingulo‐opercular network; DMN, default mode network; FPN, fronto‐parietal network; L, left; OcN, occipital network; SMN, sensorimotor network; R, right
FIGURE 5
FIGURE 5
Network‐wise contribution. (a) Normalized network‐level degree of association with ASB. Blue bars indicate the network‐level contributions by the negatively correlated dFC only, and red bars indicate the network‐level contributions by the positively correlated dFC only. Dashed bars indicate contributions of intra‐network dFC, and solid bars indicate contributions of inter‐network dFC; (b) The contribution of each pairwise inter‐network connections to the ASB‐brain association by the negatively correlated dFC only; and (c) The contribution of each pairwise inter‐network connections to the ASB‐brain association by the positively correlated dFC only. CereN, cerebellum; CON, cingulo‐opercular network; DMN, default mode network; FPN, fronto‐parietal network; OcN, occipital network; SMN, sensorimotor network
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