Neural emotion regulation during pregnancy: An fMRI study investigating a transdiagnostic mental health factor in healthy first-time pregnant women

Abstract

Pregnancy is a psycho-neuro-endocrinological transition phase presenting a window of vulnerability for mental health. Emotion regulation, a transdiagnostic factor for psychopathology, is influenced by estradiol across the menstrual cycle on the behavioral and neural level. Whether this is also the case in the antepartum period remains unknown. For the first time, behavioral and neural emotion regulation were investigated in healthy pregnant females with extremely high estradiol levels during the second trimester (N= 15) using a functional magnetic resonance imaging (fMRI) paradigm. Results were compared with naturally cycling females with high (N= 16) and low estradiol levels (N= 16). Although pregnant females reported the lowest trait use of cognitive reappraisal, all participants successfully regulated their emotions by applying cognitive reappraisal in the scanner. During downregulation of negative emotions, all females had increased activity in the left middle frontal gyrus. Pregnant females showed no significant differences in functional connectivity (psychophysiological interaction, resting-state) related to emotion regulation compared with the nonpregnant groups. However, group differences emerged for amygdala activation. In pregnant females, increased amygdala activity predicted reduced regulation success and was positively associated with depression scores. This first fMRI study during pregnancy indicates that depression scores are reflected in heightened amygdala activity already observable in the antepartum period. Thus, through its association with reduced regulation success, increased amygdala activity suggests a neural risk marker for peripartum mental health. The findings highlight the importance of investigating neural and behavioral emotion regulation in the ante- and postpartum period, eventually allowing enhanced identification, prevention, and treatment of peripartum mental ill-health.

Keywords: emotion regulation; fMRI; functional neuroimaging; peripartum mental health; pregnancy.

Fig. 1.

Study procedure (a) and negative emotion regulation paradigm (b).Note.(a) Study procedure. All participants were screened for past or present mental disorders (SCID;Beck et al., 1996;Wittchen et al., 1997) and cognitive abilities were assessed (verbal intelligence, WST;Schmidt & Metzler, 1992; processing speed and cognitive flexibility, TMT-A/B;Reitan, 1956). NC participants were randomized to receive either an E2 valerate or placebo pill 2–5 days after the onset of their menstruation and 1 day before the fMRI session (day 1). On the following day (day 2), NC females had a second pill intake 6 h before the fMRI session to maintain high E2 levels. In the fMRI session (day 2), all females performed the negative emotion regulation paradigm while being in the MRI scanner and the positive emotion regulation paradigm outside the scanner. The following self-report measures were assessed: alexithymia (TAS-20;Bach et al., 1996), self-esteem (RSES;Rosenberg, 1965;von Collani & Herzberg, 2003), state and trait anxiety (STAI;Laux et al., 1981;Spielberger, 2010), subjective affect (ESR;Schneider et al., 1994), sleep quality (PSQI;Buysse et al., 1989), body shape perception (FFB;Pook et al., 2002), sexual function (FSFI;Rosen et al., 2000), trait use of emotion regulation strategies (ERQ;Abler & Kessler, 2009;Gross & John, 2003), and depressive symptoms in pregnant (EPDS;Cox et al., 1987;Herz, 1996) and NC females (BDI-2;Beck et al., 1996;Kühner et al., 2007). Results of measurements indicated in bold are reported in the present study. (b) Negative emotion regulation paradigm. At the beginning of each trial, participants were instructed to eitherview(indicated by an equal sign) highly negative pictures or todownregulatetheir emotional response (indicated by a downward-pointing arrow) in randomized order. Pictures taken from the International Affective Picture System (Lang & Bradley, 2007) were presented on black background with a size of 800 × 600 pixels and a visual angle of 32°x24° and were followed by a jittered fixation cross. After each picture, participants rated how they felt on a continuous scale ranging from very negative to very positive. Figure adapted fromRehbein et al. (2021). BDI-2, Beck-Depression-Inventory-2; E2, estradiol; E2V, estradiol valerate; EPDS, Edinburgh Postnatal Depression Scale; ERQ, Emotion Regulation Questionnaire; ESR, Emotional Self-Rating; FFB, Fragebogen zum Figurbewusstsein (Body Shape Questionnaire); FSFI, Female Sexual Function Index; NC, naturally cycling; PSQI, Pittsburgh Sleep Quality Index; RSES, Rosenberg self-esteem scale; SCID, Structured Clinical Interview; STAI, State Trait Anxiety Index; TAS-20, Toronto Alexithymia Scale; TMT-A/B, trail making test A/B; WST, Wortschatztest (vocabulary test).

Fig. 2.

Emotional functions: Behavioral paradigm and self-report measures.Note. Left:Negative emotion regulation paradigm. Reduced negative emotional states were reported after the downregulation as compared with the view instruction across all groups. No significant differences between the groups emerged.Right: Cognitive reappraisal (ERQ); reduced self-report use of cognitive reappraisal in pregnant females compared with the placebo group. For statistical outcomes seeTable 1. Data are the median (line) and interquartile range (box) per group with lower and upper quartile as error bars. *p< .05. ERQ, Emotion Regulation Questionnaire.

Fig. 3.

Whole-brain (a) and ROI analyses (b).Note.(a) Whole-brain analysis. Contrast downregulation > view; higher brain activation during downregulation was detected in the left MFG. The bar graph shows the mean activation per group and regulation condition with standard errors as error bars. (b) ROI analyses. A tendency for a main effect of regulation was found for the left MFG with increased activity during downregulation compared with view; a significant main effect of group was found for the left amygdala and a tendency for a main effect of group found for the right amygdala. The bar graphs show the mean activation per group and regulation conditions with standard errors as error bars and individual data points. Coordinates are presented in MNI space. Results of the ANOVA effect: *p< .025, +p= .034, ‡ = .075. MFG, middle frontal gyrus; ROI, region of interest.

Fig. 4.

Relations of amygdala activity during downregulation, negative emotion regulation success, and antepartum depressive scores (EPDS).Note. (a) Amygdala activity and regulation success. Increased left amygdala activity during downregulation significantly predicts reduced regulation success in pregnant females. (b) Amygdala activity and antepartum depressive scores (EPDS) in pregnant females.Left: Increased activity in the left amygdala during downregulation was significantly related to higher EPDS scores.Right: Increased activity in the right amygdala during downregulation was significantly associated with higher EPDS scores. Coordinates are presented in MNI space. *p< .025, +p< .05. EPDS, Edinburgh Postnatal Depression Scale.