Negative bias effects during audiovisual emotional processing in major depression disorder

Abstract

Aberrant affective neural processing and negative emotional bias are trait-marks of major depression disorders (MDDs). However, most research on biased emotional perception in depression has only focused on unimodal experimental stimuli, the neural basis of potentially biased emotional processing of multimodal inputs remains unclear. Here, we addressed this issue by implementing an audiovisual emotional task during functional MRI scanning sessions with 37 patients with MDD and 37 gender-, age- and education-matched healthy controls. Participants were asked to distinguish laughing and crying sounds while being exposed to faces with different emotional valences as background. We combined general linear model and psychophysiological interaction analyses to identify abnormal local functional activity and integrative processes during audiovisual emotional processing in MDD patients. At the local neural level, MDD patients showed increased bias activity in the ventromedial prefrontal cortex (vmPFC) while listening to negative auditory stimuli and concurrently processing visual facial expressions, along with decreased dorsolateral prefrontal cortex (dlPFC) activity in both the positive and negative visual facial conditions. At the network level, MDD exhibited significantly decreased connectivity in areas involved in automatic emotional processes and voluntary control systems during perception of negative stimuli, including the vmPFC, dlPFC, insula, as well as the subcortical regions of posterior cingulate cortex and striatum. These findings support a multimodal emotion dysregulation hypothesis for MDD by demonstrating that negative bias effects may be facilitated by the excessive ventral bottom-up negative emotional influences along with incapability in dorsal prefrontal top-down control system.

Keywords: audiovisual emotional processing; major depression disorder; negative bias effects.

FIGURE 1

Experimental paradigm. Emotional stimuli were presented audiovisually, and participants were instructed to classify the emotional category of sound as soon as possible while keeping their eyes on a fixed background picture (which had two types of emotional valence: positive background, PB, or negative background, NB). The positive background (PB) and negative background (NB) were presented using a happy face (top) and sad face (bottom), respectively. Audio stimuli were randomly presented and balanced for the emotional category. The response window began with the stimulus onset. Without depending on response time, the trial duration was 4, 6, or 8 s

FIGURE 2

Functional magnetic resonance imaging activation of the full interaction of group × condition (contrast: emotionally incongruent vs. emotionally congruent). Significant post hoc comparisons of neural responsiveness (mean, square deviation) were calculated within each group and condition. Bar charts showed that the MDD group showed significantly decreased activation in the right dorsolateral prefrontal cortex, right angular gyrus, and middle occipital gyrus (contrast: IC vs. C) compared with HC in both the PB and the NB condition. Interestingly, in the left vmPFC, MDD patients showed stronger activation when one sensory channel was negative (i.e., PB with crying) under positive background. Under negative background conditions, MDD patients showed higher activation, when both sensory channels are negative (i.e., NB with crying)

FIGURE 3

Psychophysiological interaction (vmPFC; seed region) of the full interaction of group × condition (contrast: emotionally incongruent vs. emotionally congruent). Significant post hoc comparisons of neural responsiveness (mean, square deviation) were calculated within each group and condition. Bar charts showed that vmPFC showed significantly decreased connectivity with the right insula, right ventromedial prefrontal cortex, left dorsolateral prefrontal cortex, right ventrolateral prefrontal gyrus and right parahippocampal gyrus in the PB condition in the MDDs compared with HC. Diminished connectivity was found between vmPFC and right insula, right dorsolateral prefrontal cortex, right parahippocampal gyrus, left dorsolateral prefrontal cortex, right ventromedial prefrontal cortex and the right posterior cingulate cortex in the NB condition in the depression group. Importantly, MDD showed a bias in vmPFC connectivity with the right posterior cingulate cortex when participants were exposed to concurrent negative auditory information and visual facial expression stimuli

FIGURE 4

Psychophysiological interaction (dlPFC; seed region) of the full interaction of group × condition (contrast: emotionally incongruent vs. emotionally congruent). Significant post hoc comparisons of neural responsiveness (mean, square deviation) were calculated within each group and condition. Compared to the HC, the dlPFC in MDDs showed distinct decreased connectivity with the left middle temporal gyrus, left putamen, left insula, right insula, right ventrolateral prefrontal cortex and right dorsolateral prefrontal cortex in the PB condition. Increased connectivity was found in the NB condition in the depression group between the dlPFC and right putamen, left putamen, right insula, right ventrolateral prefrontal cortex and the right dorsolateral prefrontal cortex. Interestingly, under positive background conditions, MDD patients showed a bias decreased tendency in dlPFC connectivity with the bilateral putamen, bilateral insula, right ventrolateral prefrontal cortex and the right dorsolateral prefrontal cortex when participants were exposed to concurrent negative auditory information and visual facial expression stimuli