The impact of torture on interpersonal threat and reward neurocircuitry

Abstract

Objective: Torture adversely influences emotional functioning, but the neurophysiological mechanisms underpinning its impact are unknown. This study examined how torture exposure affects the neural substrates of interpersonal threat and reward processing. Methods: Male refugees with ( N = 31) and without ( N = 27) torture exposure completed a clinical interview and functional magnetic resonance imaging scan where they viewed fear, happy and neutral faces. Between-group activations and neural coupling were examined as moderated by posttraumatic stress disorder symptom severity and cumulative trauma load. Results: Posttraumatic stress disorder symptom severity and trauma load significantly moderated group differences in brain activation and connectivity patterns. Torture survivors deactivated the ventral striatum during happy processing compared to non-torture survivor controls as a function of increased posttraumatic stress disorder symptom severity – particularly avoidance symptoms. The ventral striatum was more strongly coupled with the inferior frontal gyrus in torture survivors. Torture survivors also showed left hippocampal deactivation to both fear and happy faces, moderated by trauma load, compared to controls. Stronger coupling between the hippocampus and frontal, temporoparietal and subcortical regions during fear processing was observed, with pathways being predicted by avoidance and hyperarousal symptoms. Conclusion: Torture exposure was associated with distinct brain activity and connectivity patterns during threat and reward processing, dependent on trauma exposure and posttraumatic stress disorder symptom severity. Torture appears to affect emotional brain functioning, and findings have the potential to guide more targeted interventions for torture survivors.

Torture exposure and the functional brain: investigating disruptions to intrinsic network connectivity using resting state fMRI

“…These findings complement existing task-related and structural MRI studies, although we note that this is the first study to observe resting-state network functioning differences in torture survivors. For example, a task-related fMRI study observed stronger lateral prefrontal cortical (part of the CEN)—hippocampus coupling during threat face processing in male torture survivors compared to non-torture survivors, as moderated by level of non-torture PTE exposure [ 26 ]. Other structural brain studies focusing on childhood maltreatment have demonstrated that dorsolateral prefrontal cortex volume diminishes following trauma [ 61 ]—a finding that is consistent with studies in torture survivors that have demonstrated grey matter volume reductions across the brain including the prefrontal cortex [ 22 , 23 ].…”

“…This is consistent with the fact that we did not identify a salience network active in our study. Our findings highlight a possible brain network-based mechanism behind this over-regulation response - that is, increased CEN-DMN dynamic functional connectivity, with possible consequences including emotional rigidity, inflexibility, withdrawal, problems with self-regulation and difficulties responding to positive interpersonal situations [ 62 ], all of which have been observed in torture survivors [ 26 ]. Torture exposure itself may therefore fundamentally alter the way intrinsic networks of the brain—in particular the CEN and DMN—function and connect.…”

“…For example, studies have reported volumetric changes [ 21 , 22 ], cortical thinning [ 23 ] and white matter connectivity differences [ 21 ] in torture survivors with PTSD compared to healthy controls, with the degree of structural differences being associated with trauma exposure [ 22 ] or depression symptoms [ 23 ]. Functional studies have shown that torture survivors with PTSD differentially engage threat-related, emotion regulation [ 24 – 26 ] or sensory processing [ 27 , 28 ] brain systems compared to either torture survivors without PTSD or healthy controls [ 16 ]. The prefrontal cortex may be particularly affected by torture exposure, both structurally [ 22 , 23 ] and functionally [ 24 , 26 ].…”

“…Functional studies have shown that torture survivors with PTSD differentially engage threat-related, emotion regulation [ 24 – 26 ] or sensory processing [ 27 , 28 ] brain systems compared to either torture survivors without PTSD or healthy controls [ 16 ]. The prefrontal cortex may be particularly affected by torture exposure, both structurally [ 22 , 23 ] and functionally [ 24 , 26 ]. While these studies have afforded some insights into the neural effects of torture, the derivation of robust conclusions has been difficult because of methodological variation between studies [ 16 ], which include: (1) the nature of participant groupings, which have lacked a specific focus on torture exposure itself by either including participants with exposure to multiple conflict-related events including torture in the one group [ 22 , 24 , 25 , 29 ], not distinguishing between torture exposure and PTSD diagnosis [ 21 , 22 ], or else comparing torture survivors to healthy controls without torture histories [ 22 , 24 ], which may exaggerate the specific effects of torture [ 16 ]; (2) the focus on fMRI and MEG studies with task-related designs, which precludes insights into how torture affects the functional dynamics of brain networks.…”

“…In this study, we examined how torture exposure modulates functional connectivity within and between the three networks of the triple network model comprising the DMN, SN and CEN, as well as any prefrontal cortical network due to prior evidence that its functioning is affected by torture [ 24 – 26 ]. To overcome previously identified methodological issues and to focus directly on the effects of torture exposure, we recruited a sample of torture survivors with a refugee background as the target group, and a comparison group comprising refugees without a history of torture exposure, while statistically controlling for PTSD symptoms and exposure to non-torture PTEs.…”