Emotion, as well as cognition, are often understood as a manifestation of brain activity. However, bodily processes are also involved in mental functioning, referring to the concept of embodiment. Embodied emotion, traditionally, implies that experiencing an emotion involves perceptual, somato-visceral, and motor aspects. Within the frame of the Research Training Group “Situated Cognition”, we here extend the concept of embodiment by considering the role of hormones in the processing of emotional content. Importantly, hormones allow a bidirectional body-to-brain and brain-to-body coupling. The endocrine system, e.g., steroid sex hormones, produced in the gonads, send feedback to the brain by binding at their receptors. These receptors are relatively abundant in the brain regions associated with emotional processing, memory, and executive functions (i.e., amygdala, hippocampus, and prefrontal cortex). Moreover, peripheral hormone secretion is modulated via actions from the central nervous system. We intended to characterize the role of sex hormones, and partly also of stress hormones, on different components of emotion as a hormonal embodiment of emotion.
Thus, we examined emotional processing in different sex hormone-status groups. To account for different levels of sex hormones, we used a quasi-experimental approach by comparing women in different cycle phases, women using hormonal oral contraceptives (Study 1), and additionally men (in Study 2). The female menstrual cycle is characterized by fluctuating sex hormone levels. On the peripheral gonadal level, these are 17β-estradiol and progesterone. These hormones are low at the beginning of the cycle (early follicular phase). Estradiol rises towards the middle of the cycle (mid-cycle) and stays moderately high until the next cycle. Progesterone levels are high after mid-cycle in the luteal phase until the end of the cycle. Hormonal contraceptives suppress the endogenous production of estradiol and progesterone, keeping the hormone levels low during the whole cycle. Estradiol and progesterone are also present in males, however, at low levels with no sign of cyclical fluctuations.
In Study 1, we examined three independent groups of women in the mid-cycle (n = 24), in the luteal phase (n = 24), and women using hormonal oral contraceptives (n = 24). We assessed different measures of emotional processing, i. e. emotional memory, cognitive and affective empathy-related measures (emotion recognition and ratings for feeling with a protagonist´s emotion, respectively), as well as mimic and skin-conductance responses to affective stimuli. Additionally, we addressed interactions of experimental stress (cold pressor test vs. control) with sex hormones in emotional memory. Our data demonstrated the role of hormones in empathy-related measures and skin-conductance responses depending on the stimulus characteristics (valence, the gender of the protagonist). Emotional memory was not affected by hormone status, stressor or salivary hormone levels. In the cognitive empathy-related measure, women in the luteal phase, as well as oral contraceptive users, identified emotions depicted by female protagonists more accurately than those by male protagonists. On the other hand, estradiol correlated positively with recognition of emotions depicted by males in the total sample. In the affective empathy-related measure, oral contraceptive users rated negative emotions higher than the positive ones. Finally, in the luteal phase skin-conductance responses to negative stimuli were heightened, also supported by a positive correlation with the salivary progesterone levels. The mimic responses remained unaffected. None of the remaining associations with the salivary hormone levels were significant. These results indicate that sex hormones modulated emotional processing by interacting with the stimulus features, as evident in the negativity bias under oral contraceptive use and in the luteal phase in the affective empathy-related measure and sympathetic autonomous reactivity, respectively. However, emotional memory and mimic activity to affective stimuli were not affected.
In Study 2, we extended the initial scope to examine the role of sex hormones and olfaction in empathy-related measures. Reports of female advantage in empathy-related measures suggest a role for sex hormones, although data are inconsistent. Studies also report similar sex differences in human olfactory perception. In rodents, olfaction is involved in detecting and integrating socially-relevant information and is modulated by the brain-actions of estrogens. Based on this background, we hypothesized that olfaction may untangle the mixed evidence regarding the relationship between sex hormones and empathy-related measures (cognitive, affective). Thus, we measured odor discrimination ability, empathy-related measures, and facial mimic activity (also associated with affective empathy-related measures) in free-cycling women in high sex-hormone phases (n = 20), oral contraceptive users (n = 19), and men (n = 21). Free-cycling women outperformed only men in the recognition of emotions depicted from the eye region. Oral contraceptive users showed higher scores in the affective empathy-related measure towards negative emotions. Free-cycling women exhibited the strongest facial mimicry (viewing female, but not male protagonists), positively associated with progesterone. Finally, the groups differed in odor discrimination, with free-cycling women outperforming men. However, odor discrimination ability and empathy-related performance were not correlated. Our results support the role of sex hormones in odor perception and empathy-related measures, to a certain extent. However, no common underlying mechanism was found.
Finally, we conducted a systematic review (Study 3) aiming to elucidate factors contributing to the inconsistent results concerning the role of sex hormones in the two most addressed areas of emotional processing, emotion recognition (empathy-related measure) and emotional memory. Thereby, we extended previous reviews that address single areas of emotion processing. Moreover, we systematically addressed the role of situational features (mainly emotion-type and/or stimulus valence). All studies included healthy women of reproductive age either in stages of their natural menstrual cycle or using oral contraceptives, and measured or at least estimated levels of ovarian sex hormones. We document the methodological diversity in the field, presumably contributing to the heterogeneity of results. We recognized the need for studies explicitly contrasting the early follicular, mid-cycle, and mid-luteal phases, as well as OC-intake and using standardized tasks. Research would take advantage of using within-subject design more frequently and account for the recognition of complex emotions.
In sum, our data suggest that sex hormones differentially modulate the cognitive and affective empathy-related performance and skin-conductance responses by interacting with situational variables, such as the emotional valence of the stimuli and the gender of the protagonist. Women in the luteal phase and under oral contraceptive use demonstrated better recognition of emotions depicted by female protagonists. By contrast, estradiol levels positively correlated with the recognition of emotions depicted by male protagonists. Sex-hormone status main effects only manifested in the emotion recognition advantage of free-cycling women over men (Reading the Mind in The Eyes Test; Study 2). In both studies, affective empathy ratings towards negative emotions were higher in the oral contraceptive users. Moreover, although mimic activity was not associated with sex hormones, skin-conductance responses to negative stimuli were heightened in the luteal phase. On the other hand, the performance in empathy-related measures in different hormone-status groups was not related to odor discrimination ability. Additionally, the inconsistencies of the sex hormone and emotion research could be the result of variations of designs and tasks used across studies from a similar field. This is also indicated in our findings from the empathy-related measures differing in tasks and hormone-status groups in two studies. Finally, our findings provide evidence that emotional processes under sex-hormone modulation are situated, i.e., subject to the influence of the stimulus valence. Furthermore, they are embodied via coupling between the endocrine system and the brain as evident in hormone status and valence interactions in empathy-related measures and sympathetic reactivity.
| Identifer | oai:union.ndltd.org:uni-osnabrueck.de/oai:repositorium.ub.uni-osnabrueck.de:urn:nbn:de:gbv:700-202106155132 |
| Date | 15 June 2021 |
| Creators | Gamsakhurdashvili, Dali |
| Contributors | Prof. Dr. Ursula Stockhorst, Prof. Dr. Onur Güntürkün |
| Source Sets | Universität Osnabrück |
| Language | English |
| Detected Language | English |
| Type | doc-type:doctoralThesis |
| Format | application/pdf, application/zip |
| Rights | Attribution-NonCommercial-NoDerivs 3.0 Germany, http://creativecommons.org/licenses/by-nc-nd/3.0/de/ |
Page generated in 0.003 seconds