Impaired salience network switching in psychopathy

Abstract

Growing evidence suggests that psychopathy is related to altered connectivity within and between three large-scale brain networks that support core cognitive functions, including allocation of attention. In healthy individuals, default mode network (DMN) is involved in internally-focused attention and cognition such as self-reference. Frontoparietal network (FPN) is anticorrelated with DMN and is involved in externally-focused attention to cognitively demanding tasks. A third network, salience network (SN), is involved in detecting salient cues and, crucially, appears to play a role in switching between the two anticorrelated networks, DMN and FPN, to efficiently allocate attentional resources. Psychopathy has been related to reduced anticorrelation between DMN and FPN, suggesting SN's role in switching between these two networks may be diminished in the disorder. To test this hypothesis, we used independent component analysis to derive DMN, FPN, and SN activity in resting-state fMRI data in a sample of incarcerated men (N = 148). We entered the activity of the three networks into dynamic causal modeling to test SN's switching role. The previously established switching effect of SN among young, healthy adults was replicated in a group of low psychopathy participants (posterior model probability = 0.38). As predicted, SN's switching role was significantly diminished in high psychopathy participants (t(145) = 26.39, p < .001). These findings corroborate a novel theory of brain function in psychopathy. Future studies may use this model to test whether disrupted SN switching is related to high psychopathy individuals' abnormal allocation of attention.

Keywords: Dynamic causal modeling; MRI; Neuroimaging; Psychopathy; Salience network.

Figure 1.

Three fully connected DCM models specified for each participant and compared using random-effects Bayesian model selection. Sets of black arrows represent bidirectional connectivity between each network. Red arrows represent one network’s modulatory effect on the connectivity between the other two networks. DMN = default mode network, FPN = frontoparietal network, SN = salience network

Figure 2.

Components derived from the constrained ICA, averaged across subjects. The first component corresponded to default mode network (DMN; A), the second component corresponded to frontoparietal network (FPN; B), and the third component corresponded to salience network (SN; C). The most inferior slice in each panel is z = −30, the most superior slice is z = 70, and each slice is separated by five mm. Voxels with significant (uncorrected p < .001, p_FWE < .05, cluster extent threshold = 27 voxels) t-values (displayed in the color bar) are shown.

Figure 3.

Posterior model probabilities and exceedance probabilities for the low psychopathy group (PCL-R ≤ 20). DMN = default mode network, FPN = frontoparietal network, SN = salience network

Figure 4.

A) Posterior model probabilities for the SN modulation model in the low (PCL-R ≤ 20), intermediate (PCL-R > 20 and < 30), and high (PCL-R ≥ 30) psychopathy groups. B) Estimates from the SN modulation model of the modulatory effect of SN on DMN-to-FPN connectivity (left) and FPN-to-DMN connectivity (right) in the low, intermediate, and high psychopathy groups. In both panels, error bars represent 1 standard error above and below the point estimate of the reference-coded model comparing the high psychopathy group to the low and intermediate psychopathy groups. DMN = default mode network, FPN = frontoparietal network, SN = salience network, * p < .05, *** p < .001