Free-viewing gaze patterns reveal a mood-congruency bias in MDD during an affective fMRI/eye-tracking task

Abstract

Major depressive disorder (MDD) has been related to abnormal amygdala activity during emotional face processing. However, a recent large-scale study (n = 28,638) found no such correlation, which is probably due to the low precision of fMRI measurements. To address this issue, we used simultaneous fMRI and eye-tracking measurements during a commonly employed emotional face recognition task. Eye-tracking provide high-precision data, which can be used to enrich and potentially stabilize fMRI readouts. With the behavioral response, we additionally divided the active task period into a task-related and a free-viewing phase to explore the gaze patterns of MDD patients and healthy controls (HC) and compare their respective neural correlates. Our analysis showed that a mood-congruency attentional bias could be detected in MDD compared to healthy controls during the free-viewing phase but without parallel amygdala disruption. Moreover, the neural correlates of gaze patterns reflected more prefrontal fMRI activity in the free-viewing than the task-related phase. Taken together, spontaneous emotional processing in free viewing might lead to a more pronounced mood-congruency bias in MDD, which indicates that combined fMRI with eye-tracking measurement could be beneficial for our understanding of the underlying psychopathology of MDD in different emotional processing phases.Trial Registration: The BeCOME study is registered on ClinicalTrials (gov: NCT03984084) by the Max Planck Institute of Psychiatry in Munich, Germany.

Keywords: A mood-congruency bias; Emotional processing; Eye-tracking; Free-viewing; Major depressive disorder; fMRI.

Fig. 1

a Schematic representation of the experimental procedure. The task included eight blocks (four blocks for emotional faces (*) and the other four blocks for geometric forms (^#)), each with six trials. In each trial, a stimulus with three objects (emotional faces presenting for 6 s and geometric forms presenting for 4 s) was displayed after a fixation cross (1.8–2.3 s). During the presentation of the stimulus, participants were instructed to press the corresponding button according to emotional expression or shape. b Schematic illustration of the task-related phase (TRP) and the free-viewing phase (FVP). The two phases were allocated based on the response timing in a trial with 6 s (emotion recognition) or 4 s (shape recognition). TRP was defined as the time from the start of the stimulus display to the behavioral response (button press), while FVP was defined as the time from the behavioral response to the end of the trial (stimulus offset). The facial stimuli are reproduced with permission from the Paul Ekman Group

Fig. 2

Response times (RT) for a different stimulus types and emotional pairs (i.e., happy–negative and negative–negative pairs); b the specific emotional stimulus pairings. Error bars denote standard errors. ***p < 0.001. ms milliseconds

Fig. 3

Interactions between group and the specific-valenced pair in the task-related phase (a) and the free-viewing phase (b). In the free-viewing phase, MDD patients had lower PTRA for happy–sad pairs than other mixed-emotional pairs, indicating that they had more attentional preferences for sad faces than other negative ones. Error bars denote standard errors. ***p < 0.001. MDD major depressive disorder, HC healthy control

Fig. 4

Brain activity between stimulus types analyzed separately for the task-related phase (a) and the free-viewing phase (b). Hot colors indicate a higher BOLD response to emotional faces compared with geometric forms; cold colors refer to the inverse contrast. The background template is a mean T1-weighted image with DARTEL spatial normalization. L = left, R = right. Color bars indicate T values. p_FWE < 0.05, k > 30

Fig. 5

Brain activation (a) and neural correlates of PTRA (b) for each emotional face. Hot (cold) colors refer to more (less) activation in the free-viewing phrase compared to the task-related phase. The background template is a mean T1-weighted image with DARTEL spatial normalization. L = left, R = right. Color bars indicate T values. p_FWE < 0.05, k > 30