Childhood maltreatment is associated with lower exploration and disrupted prefrontal activity and connectivity during reward learning in volatile environments

IF 6.5 1区 医学 Q1 PSYCHIATRY
Diana J. N. Armbruster-Genç, Louise Neil, Vincent Valton, Harriet Phillips, Georgia Rankin, Molly Sharp, Jessica Rapley, Essi Viding, Jonathan P. Roiser, Eamon McCrory
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Abstract

Background

Atypical reward processing is implicated in a range of psychiatric disorders associated with childhood maltreatment and may represent a latent vulnerability mechanism. In this longitudinal study, we investigated the impact of maltreatment on behavioural and neural indices of reward learning in volatile environments and examined associations with future psychopathology assessed 18 months later.

Methods

Thirty-seven children and adolescents with documented histories of maltreatment (MT group) and a carefully matched group of 32 non-maltreated individuals (NMT group) aged 10–16 were presented with a probabilistic reinforcement learning task featuring a phase of stable and a phase of volatile reward contingencies. Brain activation and connectivity were assessed simultaneously using functional magnetic resonance imaging (fMRI). Computational models were used to extract individual estimates of learning rates and temperature, and neural signals in prespecified regions of interest were analysed during volatile and stable environments. In regression analyses, behavioural measures and neural signals at baseline were used to predict psychological symptoms at follow-up.

Results

The MT group showed lower behavioural exploration, which predicted decreased internalising symptoms at follow-up. The MT group had lower activation in the orbitofrontal cortex (OFC) during outcome delivery in volatile relative to stable contexts. OFC connectivity with an area in the mid-cingulate cortex was also lower during outcome processing, which predicted higher general psychopathology at follow-up.

Conclusions

These findings are consistent with the notion that low exploratory behaviour following childhood maltreatment is potentially a protective adaptation against internalising symptoms, while disrupted neural processing of reward learning in volatile environments may index latent vulnerability to mental illness.

Abstract Image

在不稳定的环境中,儿童虐待与探索能力降低、前额叶活动和连接中断有关。
背景:非典型奖励加工涉及一系列与儿童虐待相关的精神疾病,可能代表一种潜在的脆弱性机制。在这项纵向研究中,我们调查了虐待对不稳定环境中奖励学习的行为和神经指标的影响,并检查了18个月后评估的未来精神病理的关系。方法:37名有虐待史的儿童和青少年(MT组)和32名年龄在10-16岁的未受虐待的儿童和青少年(NMT组)被提出了一个概率强化学习任务,该任务具有稳定和不稳定奖励随因的阶段。使用功能磁共振成像(fMRI)同时评估大脑激活和连通性。计算模型用于提取学习率和温度的个体估计,并在波动和稳定的环境中分析预先指定的感兴趣区域的神经信号。在回归分析中,基线时的行为测量和神经信号用于预测随访时的心理症状。结果:MT组表现出较低的行为探索,这预示着随访时内化症状的减少。MT组在结果传递过程中,眼窝额叶皮质(OFC)的激活程度较低。在结果处理过程中,OFC与中扣带皮层区域的连通性也较低,这预示着随访时更高的一般精神病理。结论:这些发现与以下观点一致:儿童虐待后的低探索性行为可能是一种针对内化症状的保护性适应,而在不稳定的环境中,奖励学习的神经加工被破坏可能表明对精神疾病的潜在脆弱性。
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来源期刊
CiteScore
13.80
自引率
5.30%
发文量
169
审稿时长
1 months
期刊介绍: The Journal of Child Psychology and Psychiatry (JCPP) is a highly regarded international publication that focuses on the fields of child and adolescent psychology and psychiatry. It is recognized for publishing top-tier, clinically relevant research across various disciplines related to these areas. JCPP has a broad global readership and covers a diverse range of topics, including: Epidemiology: Studies on the prevalence and distribution of mental health issues in children and adolescents. Diagnosis: Research on the identification and classification of childhood disorders. Treatments: Psychotherapeutic and psychopharmacological interventions for child and adolescent mental health. Behavior and Cognition: Studies on the behavioral and cognitive aspects of childhood disorders. Neuroscience and Neurobiology: Research on the neural and biological underpinnings of child mental health. Genetics: Genetic factors contributing to the development of childhood disorders. JCPP serves as a platform for integrating empirical research, clinical studies, and high-quality reviews from diverse perspectives, theoretical viewpoints, and disciplines. This interdisciplinary approach is a key feature of the journal, as it fosters a comprehensive understanding of child and adolescent mental health. The Journal of Child Psychology and Psychiatry is published 12 times a year and is affiliated with the Association for Child and Adolescent Mental Health (ACAMH), which supports the journal's mission to advance knowledge and practice in the field of child and adolescent mental health.
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