Childhood Trauma, Brain Structure and Emotion Recognition in Patients With Schizophrenia and Healthy Participants

Karolina I. Rokita; Laurena Holleran; Maria R. Dauvermann; David Mothersill; Jessica Holland; Laura Costello; Ruán Kane; Declan McKernan; Derek W. Morris; John P. Kelly; Aiden Corvin; Brian Hallahan; Colm McDonald; Gary Donohoe

Disclosures

Soc Cogn Affect Neurosci. 2020;15(12):1336-1350. 

In This Article

Abstract and Introduction

Abstract

Childhood trauma, and in particular physical neglect, has been repeatedly associated with lower performance on measures of social cognition (e.g. emotion recognition tasks) in both psychiatric and non-clinical populations. The neural mechanisms underpinning this association have remained unclear. Here, we investigated whether volumetric changes in three stress-sensitive regions—the amygdala, hippocampus and anterior cingulate cortex (ACC)—mediate the association between childhood trauma and emotion recognition in a healthy participant sample (N = 112) and a clinical sample of patients with schizophrenia (N = 46). Direct effects of childhood trauma, specifically physical neglect, on Emotion Recognition Task were observed in the whole sample. In healthy participants, reduced total and left ACC volumes were observed to fully mediate the association between both physical neglect and total childhood trauma score, and emotion recognition. No mediating effects of the hippocampus and amygdala volumes were observed for either group. These results suggest that reduced ACC volume may represent part of the mechanism by which early life adversity results in poorer social cognitive function. Confirmation of the causal basis of this association would highlight the importance of resilience-building interventions to mitigate the detrimental effects of childhood trauma on brain structure and function.

Introduction

The ability to recognise emotional facial expressions is a highly developed and integral feature of social cognition, and an important predictor of socio-occupational functioning, contributing to quality of life (Fett et al., 2011; Fiszdon et al., 2013). Impairments in emotion recognition have been particularly well-documented in psychiatric disorders, such as schizophrenia (SZ), which is characterised by wide-ranging social cognitive deficits (Mier and Kirsch, 2017). Individual differences in emotion recognition have also been found in healthy samples with lower age and higher education level leading to a better ability to recognise facial expressions (Isaacowitz et al., 2007; Tamamiya and Hiraki, 2013).

While adverse childhood experiences (i.e. emotional abuse, physical abuse, sexual abuse, emotional neglect and physical neglect) have been consistently associated with various negative outcomes across the life course, including mental health problems (Bendall et al., 2008; Mandavia et al., 2016; Morgan and Gayer-Anderson, 2016; Hébert et al., 2018), there is also growing evidence that traumatic experiences in childhood are related to deficits in the ability to recognise emotions in both clinical (e.g. SZ) and non-clinical populations (Rokita et al., 2018). Although childhood trauma is relatively common in the general population [30%; (Kessler et al., 2010)], its prevalence is particularly high in individuals with SZ [85% (Larsson et al., 2013)], with physical and emotional neglect being the most prevalent forms of child maltreatment (Stoltenborgh et al., 2013). In previous studies, we explored the possible cognitive mechanisms by which traumatic experiences in childhood may lead to social cognitive deficits in later life, in both clinical and non-clinical populations, suggesting the mediating role of attachment-related processes (Rokita et al., 2018, 2020). However, the neural substrates underlying this relationship have yet to be clarified as the specific association between childhood trauma, brain structure and social cognitive function has not yet been investigated.

Across both clinical and non-clinical samples, neuroimaging studies have found evidence that childhood trauma is associated with variability on multiple measures of brain structure and function (Heany et al., 2017; Cancel et al., 2019). On measures of brain structure, experience of childhood trauma has been linked to reductions in total grey matter volume (Cancel et al., 2015; Frissen et al., 2018; Lim et al., 2018) and volume reduction primarily in the hippocampus, amygdala, anterior cingulate cortex (ACC) and dorsolateral and ventromedial prefrontal cortices (PFCs) (Teicher et al., 2016; Cancel et al., 2019; Popovic et al., 2019) (see Supplementary Table S1 for a review of studies). Moreover, childhood trauma has been associated with changes in brain activity during emotional face tasks, mostly in the hippocampus, amygdala and ACC (Benedetti et al., 2011; Anticevic et al., 2012; van Harmelen et al., 2013; Teicher and Samson, 2016; Quide et al., 2017) as well as decreased functional connectivity between limbic (i.e. amygdala and hippocampus) and cortical (PFC and ACC) regions (Herringa et al., 2013; Cancel et al., 2017; Kraynak et al., 2019). However, brain activation during emotional face processing in individuals with high levels of childhood trauma appears to be dependent on emotional valence of faces. For instance, Aas et al. (2017) observed negativity bias in the processing of emotional faces and stronger differentiation in brain responses in a sample of patients with SZ spectrum and bipolar spectrum diagnosis, with clusters comprising the right angular gyrus, supramarginal gyrus, middle temporal gyrus and lateral occipital cortex.

Given the evidence that structural brain alterations in maltreated individuals are primarily observed in brain areas relevant for emotion processing, such as the amygdala, hippocampus and ACC, this is highly suggestive of the possible mediating effects of these structural alterations in the relationship between childhood trauma and emotion recognition.

While emotion processing has been linked to multiple brain structures and areas, including the fusiform face area, amygdala, insula, hippocampus, medial prefrontal cortex and ACC (Fujiwara et al., 2007; Adolphs, 2009; Anticevic et al., 2012; Maat et al., 2016; Szymkowicz et al., 2016; Krautheim et al., 2018) in both structural and functional imaging studies, this study will focus on three regions of interest (ROIs)—namely, the amygdala, hippocampus and ACC—as these structures show particular sensitivity to the effects of childhood trauma.

Despite substantial evidence for the impact of childhood trauma on brain structures involved in social cognition, particularly emotion recognition, the mediating effects of these regional brain alterations have never been investigated in psychiatric or healthy samples, to the best of our knowledge. The main objective of this study was to investigate the relationship between childhood trauma, brain structure and emotion recognition in both healthy participants and a clinical sample of patients with SZ to confirm the possible differential effects of adversity on regional brain volume and the ability to recognise emotions. Based on our recent systematic review and findings (Rokita et al., 2018, 2020), we tested the hypothesis that the association between higher levels of childhood trauma and poorer emotion recognition would be mediated via reduced volumes in one or more of three stress-sensitive brain regions—the hippocampus, amygdala and ACC.

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