Childhood maltreatment results in altered deactivation of reward processing circuits in depressed patients: A functional magnetic resonance imaging study of a facial emotion recognition task

Abstract

Importance and objectives: Childhood adversity is a strong risk factor for the development of various psychopathologies including major depressive disorder (MDD). However, not all depressed patients experience early life trauma. Functional magnetic resonance imaging (fMRI) studies using facial emotion processing tasks have documented altered blood-oxygen-level-dependent (BOLD) responses in specific cortico-limbic networks both in MDD patients and in individuals with a history of childhood maltreatment (CM). Therefore, a history of maltreatment may represent a key modulating factor responsible for the altered processing of socio-affective stimuli. To test this hypothesis, we recruited MDD patients with and without of maltreatment history to study the long-term consequences of childhood trauma and examined the impact of CM on brain activity using a facial emotion recognition fMRI task.

Methods: MDD patients with childhood maltreatment (MDD + CM, n = 21), MDD patients without maltreatment (MDD, n = 19), and healthy controls (n = 21) matched for age, sex and intelligence quotient underwent fMRI while performing a block design facial emotion matching task with images portraying negative emotions (fear, anger and sadness). The history of maltreatment was assessed with the 28-item Childhood Trauma Questionnaire.

Results: Both MDD and MDD + CM patients displayed impaired accuracy to recognize sad faces. Analysis of brain activity revealed that MDD + CM patients had significantly reduced negative BOLD signals in their right accumbens, subcallosal cortex, and anterior paracingulate gyrus compared to controls. Furthermore, MDD + CM patients had a significantly increased negative BOLD response in their right precentral and postcentral gyri compared to controls. We found little difference between MDD and MDD + CM patients, except that MDD + CM patients had reduced negative BOLD response in their anterior paracingulate gyrus relative to the MDD group.

Conclusions: Our present data provide evidence that depressed patients with a history of maltreatment are impaired in facial emotion recognition and that they display altered functioning of key reward-related fronto-striatal circuits during a facial emotion matching task.

Keywords: Adverse childhood experiences; CTQ; Child abuse; Childhood trauma; MRI; Major depressive disorder.

Fig. 1

Experimental design of our facial emotion recognition task with examples of images with emotional stimuli. A: After a short training session (1 trial of face and 1 trial of shape), the block design task included 6 blocks of a 30-s-long shape matching task (control) alternating with a 30-s-long face matching task (face). The face matching task contained a total of 2 fearful, 2 angry, and 2 sad faces blocks interleaved with control (shape matching) tasks. One block contained 6 sequential matching trials, each was presented for 5s with no interstimulus interval. The whole run contained a total of 12 blocks and 72 trials (6 face match and 6 shape match blocks) and it lasted for 360 s without the training session. Subjects were instructed to match one of the two test shapes or faces on the bottom that were similar (in shape) or expressed the same emotion as the target shape/face on the top of the screen. B: Representative images of faces with various emotional expressions. Each match emotion trial included a trio of male or female faces expressing neutral, fearful, angry, and sad emotions.

Fig. 2

Group level activations, i.e. face matching > shape matching contrast (A) and deactivations, i.e. shape matching > face matching contrast (B) during the facial emotion recognition task in healthy controls (HC). Images were thresholded using clusters determined by Z > 2.3 and an FWE corrected cluster significance threshold of p = 0.05. Axial slices are shown in radiological convention for MNI slice coordinates from Z = -72 mm to Z = 84 mm.

Fig. 3

Group level activations, i.e. face matching > shape matching contrast (A) and deactivations, i.e. shape matching > face matching contrast (B) during the facial emotion recognition task in MDD patients. Images were thresholded using clusters determined by Z > 2.3 and an FWE corrected cluster significance threshold of p = 0.05. Axial slices are shown in radiological convention for MNI slice coordinates from Z = -72 mm to Z = 84 mm.

Fig. 4

Group level activations, i.e. face matching > shape matching contrast (A) and deactivations, i.e. shape matching > face matching contrast (B) during the facial emotion recognition task in MDD + CM patients. Images were thresholded using clusters determined by Z > 2.3 and an FWE corrected cluster significance threshold of p = 0.05. Axial slices are shown in radiological convention for MNI slice coordinates from Z = -72 mm to Z = 84 mm.

Fig. 5

The significant results of pairwise between-group comparisons of BOLD responses during the facial emotion matching task among the three groups, i.e. Control versus MDD, Control versus MDD + CM and MDD versus MDD + CM. To account for the post-hoc character of these between-group statistical tests and to reduce the chance of false-positive findings, only those voxels are shown as significant, where the omnibus F-test also revealed a significant group effect. Significant differences were found in the negative BOLD response during the facial emotion matching task, i.e. Control > MDD + CM, MDD > MDD + CM and MDD + CM > Control, where “>” means increased negative BOLD signal. Since there were only a few differences, these are presented here in a single figure. More details about these group-differences are presented in Table 7. The images were thresholded using clusters determined by Z > 2.3 and an FWE corrected cluster significance threshold of p = 0.05. The presented results are controlled for age and sex and masked with significant F-test results (Z > 2.3, cluster-wise p < 0.05) to avoid false-positive findings. Axial slices are shown in radiological convention for MNI slice coordinates from Z = -20 to 40 mm.

Fig. 6

Group level positive associations between BOLD response and number of depressive episodes in the MDD + CM group (A) and between BOLD response and age at illness onset in MDD subjects (B) during the facial emotion matching task. Images were thresholded using clusters determined by Z > 2.3 and an FWE corrected cluster significance threshold of p = 0.05. Axial slices are shown in radiological convention for MNI slice coordinates from Z = 32–44 mm (A) and Z = -8 to 4 mm (B). Significant interaction effects were masked with the results of the F-test to avoid false-positive results.