Elsevier

Neuroscience Letters

Volume 806, 29 May 2023, 137196
Neuroscience Letters

Childhood sexual abuse related to brain activity abnormalities in right inferior temporal gyrus among major depressive disorder

https://doi.org/10.1016/j.neulet.2023.137196Get rights and content

Highlights

  • ALFF was altered in multiple brain regions of first-episode, drug-naive MDD.

  • Childhood sexual abuse (CSA) was negatively correlated with the altered ALFF in the right ITG among MDD patients.

  • ALFF in the right ITG might be a potential biomarker for MDD patients with CSA.

Abstract

Regional brain activity abnormalities have been reported in major depressive disorder (MDD) with childhood trauma (CT). However, these findings were variable and equivocal. The present study aims to explore further the correlation between CT and the amplitude of low-frequency fluctuations (ALFF) alteration in MDD. In this study, we recruited 60 healthy controls (HCs) and 66 MDD patients to complete resting-state fMRI scans. All MDD patients were evaluated clinical symptoms and childhood trauma experience using the Hamilton Depression Rating Scale-17 (HDRS-17), the Hamilton Anxiety Scale (HAMA), and the Childhood Trauma Questionnaire (CTQ). Compared to HCs, MDD patients demonstrated significantly altered ALFF in the right middle occipital gyrus (MOG), bilateral inferior temporal gyrus (ITG), bilateral cerebellum posterior lobe, bilateral anterior cingulate gyrus (ACC), and bilateral superior frontal gyrus (SFG). More importantly, we found negative correlation between childhood sexual abuse (CSA) scores and ALFF value appeared mainly in the right ITG among MDD patients. After adjusting for covariates (age, gender, mean framewise displacement (FD), HDRS-17, and HAMA scores), this correlation remained significant. Meanwhile, ALFF in the right ITG could distinguish MDD patients with or without CSA (area under the curve (AUC) = 0.713). Our findings revealed that the regional brain activity abnormalities in the right ITG might be a potential biomarker for MDD patients with CSA.

Introduction

Major depressive disorder (MDD) was considered the most common psychiatric disease worldwide, accounting for a significant portion of the global disease burden [1]. The occurrence of MDD was related to many factors, including stressful life events and circumstances, dysfunctional cognitions, and other risk factors [2]. There were many indications that depression was significantly associated with early life events, especially childhood trauma (CT) [3]. A recent meta-analysis found that trauma-exposed individuals were twice as likely as non-trauma-exposed individuals to develop both recurrent and persistent depressive episodes [4]. The adverse effect of CT on MDD varies by type of CT [3]. This has been reported that childhood abuse (CA) was significantly related to high levels of depression and anxiety [4]. Meanwhile, the impact of childhood neglect (CN) on MDD could not be ignored. Thus, it was important to elucidate the pathogenic mechanism of MDD with the different CT.

To understand the underlying mechanisms of MDD, recent research has become increasingly focused on functional magnetic resonance imaging (fMRI) [1], [5], [6]. fMRI was a popular tool for exploring brain function in psychiatric disorders and offered significant advantages over conventional recording methods [7]. It has been shown that MDD patients were more likely to develop functional brain alterations, especially abnormal regional brain activity [8]. The amplitude of low-frequency fluctuation (ALFF) was considered a reliable and sensitive indicator of regional brain activity [9]. ALFF was reported to have higher test–retest reliability of amplitude measures compared to fractional amplitude low-frequency fluctuations (fALFF) [10]. Hence, it might be more appropriate to assess regional brain activity abnormalities [11].

A recent meta-analysis indicated that MDD patients displayed ALFF alterations in multiple brain regions, including the superior frontal gyrus (SFG), supramarginal gyrus (SMG), occipital cortex, insula, striatum, cerebellum, and precuneus [8]. Notably, people with chronic trauma also showed brain activity alterations in many emotion-related brain regions [12]. These results indicated that regional brain activity abnormalities in MDD patients might be related to childhood trauma experience. However, despite some studies reporting specific brain activity alterations in MDD patients with CT, the findings were variable and equivocal in previous studies [13], [14], [15]. This result might be related to the heterogeneity of MDD patients [16]. Several studies have shown that antidepressants alter neuronal remodeling, affecting the brain structure and function [17], [18], [19]. Disease course and severity were also reported as an important reason for the heterogeneity of altered brain activity [20], [21], [22]. More importantly, the influence of different CT on the regional brain activity of MDD has been rarely investigated.

To elucidate the potential mechanisms, we would further explore the correlation between the specific altered ALFF of MDD and the different CT. In this study, only first-episode, drug-naive MDD patients were included to reduce the clinical heterogeneity. Accordingly, the study hypotheses were: Firstly, the altered ALFF was observed in multiple brain regions of MDD patients compared to healthy controls (HCs). Secondly, the ALFF alterations correlated with different CT, and this correlation persisted after adjustment for the effect of depression-associated symptoms. Finally, this specific alteration could be applied to distinguish MDD patients with or without different CT.

Section snippets

Participants

A total of 66 patients with first-episode drug-naive MDD were recruited from the Tianjin Mental Health Center. Meanwhile, 60 normal participants who were sex- and age-matched with patients were recruited as HCs. All participants were aged from 18 to 55. A Structured Clinical Interview for the Diagnostic and Statistical Manual of Mental Disorders (5th Edition) (DSM-V Axis I Disorders) was used to diagnose MDD. Exclusion criteria for MDD patients included the following: (1) other major

Clinical and demographic characteristics

Table 1 shows the clinical demographic characteristics of the subjects. In MDD patients, the mean scores of the HDRS-17 and HAMA were 23.94 ± 6.27 and 21.05 ± 6.89, respectively. The total CTQ scores were 45.15 ± 11.51 in MDD patients (CEA, 9.33 ± 4.23; CPA, 6.32 ± 2.62; CSA, 5.73 ± 1.32; CEN, 14.5 ± 4.78; CPN, 9.27 ± 3.28). There was no significant difference in age and gender between HCs and MDD patients (p > 0.05).

Regional brain activity abnormalities in MDD patients

Compared to HCs, MDD patients demonstrated significantly lower ALFF in the

Discussion

To our knowledge, this was one of the few studies to explore the association between the altered ALFF of first-episode drug-naive MDD and the different CT. This research revealed altered ALFF in multiple brain regions of MDD patients. Most importantly, we found negative correlations between CSA and the altered ALFF in the right ITG, and this result was unaffected by depressive and anxiety symptoms. Meanwhile, the ALFF in the right ITG could be applied to distinguish between MDD patients with or

Conclusion

In conclusion, the altered ALFF in multiple brain regions was found in first-episode drug-naive MDD. What is more, we found negative correlations between childhood sexual abuse and the altered ALFF in the right ITG, regardless of the severity of depression and anxiety. Meanwhile, the ALFF in the right ITG had a better performance in identifying MDD patients with CSA. Thus, we cautiously speculated that the regional brain activity abnormalities in the right ITG might be a potential biomarker for

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We would like to acknowledge all health people and MDD patients who participated in the study. This study was supported by the Tianjin Key Medical Discipline (Specialty) Construction Project (Grant: TJYXZDXK-033A), Foundation of Tianjin Health Commission for Young Scholars (Grant: KJ20025), and Tianjin Health Science and Technology Project (Grant: MS20019). The funding had no effect on the study's design, data collection, analysis, and interpretation of results.

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