Background
Enhanced processing of negative stimuli contributes to high negative affective response, enduring negative affect, and emotional disorders [
1]. It involves enhanced selective attention toward a negative stimulus relative to a neutral stimulus (i.e., attentional bias) and enhanced encoding, storage, and retrieval of negative stimuli (i.e., memory bias). Enhanced processing of negative stimuli is observed under acute psychosocial stressors [
2]. Stressors induce cortisol release, which is the final hormone of the hypothalamic–pituitary–adrenal (HPA) axis. Change in emotional information processing after stress exposure is reported to be associated with stress-induced cortisol [
3], and stress-induced cortisol is assumed to be one of the possible biological mediators between stress and enhanced emotional information processing. The brain is one of the targets of cortisol, and the prefrontal cortex, hippocampus, and amygdala have a high density of corticosteroid receptors [
4,
5]. It is assumed that cortisol could modulate emotion information processing through its actions in these areas.
Enhanced processing of emotional stimuli could make cognitive emotion regulation more difficult. Emotion regulation refers to shaping the kind of emotions that one possesses and their strength [
6]. Cognitive emotion regulation involves the alternation of ongoing emotional responses through the processing of emotional stimuli. Two types of cognitive emotion regulations have been identified, attentional control and cognitive change [
7]. Attentional control is implemented at an early information processing stage immediately following sensory intake and includes selective inattention toward negative stimuli. Cognitive change is implemented at a later and more elaborate information processing stage and includes cognitive reappraisal, which is defined as reinterpreting a stimuli or a situation in such a way as to reduce its emotional impact [
8]. Cognitive change processes involve generating and retaining non-negative interpretations while inhibiting negative interpretations of stimuli or situations that are evaluated as stressful [
9]. Therefore, enhanced information processing of negative stimuli might interfere with these cognitions.
Stress-related psychiatric disorders that include aspects of depression are related to the absence of effective use of cognitive emotion regulation [
10]. In addition, individuals with depression have been shown to generate fewer non-negative interpretations of stressful social situations [
11]. Cortisol is one of the neurobiological correlates of depression [
12], which may be partly due to the cortisol action on generation of non-negative interpretations. Although previous studies have not investigated the relation between stress-induced cortisol and cognitive reappraisal, stress-induced cortisol may be associated with impairment in the later information processing stage as well as with impairment in the earlier stage that includes attentional bias [
3].
This study aimed to investigate the relationship between stress-induced cortisol and non-negative interpretations generated to regulate depressive mood in response to depression-related stimuli. We compared changes in the generation of non-negative interpretations before and after stress induction of participants with and without cortisol elevation in response to stress induction (responders and non-responders) to examine differences in their information processing of depression-related stimuli between conditions with and without cortisol elevation. We tested the hypotheses that the responders would generate fewer non-negative interpretations than the non-responders, for whom the number would be constant.
Discussion
The study tested the hypothesis that stress-induced cortisol would be associated with the generation of fewer non-negative interpretations to depression-related stressful social situations. To test this hypothesis, we compared the change in the number of non-negative interpretations generated following the stress induction task between responders and non-responders. In responders, the number of non-negative interpretations generated decreased after the stress induction task, whereas in non-responders the number of non-negative interpretations generated was constant. Furthermore, the number of post-stress non-negative interpretations was lower for the responders than the non-responders when compared by sex, baseline cortisol level, and the number of pre-stress non-negative interpretations, statistically controlled. These results support the hypotheses. However, inconsistent with the hypothesis, our results found no significant correlation; this was probably partly due to the small sample size. Thus, the results, although inconclusive, suggest the possibility that stress-induced cortisol might be related to decreased generation of non-negative interpretations during cognitive reappraisal of depression-related stressful social situations.
A plausible mediator between increased stress-induced cortisol and a decrease in the number of non-negative interpretations generated following the stress induction task could be enhanced attentional bias toward a neutral stimulus. It has been reported that stress-induced cortisol is related to attentional bias toward negative stimuli [
3]. Attentional bias is reported to be associated with cognitive reappraisal. For instance, an eye tracking study reported that, during cognitive reappraisal, attention is more frequently oriented toward non-emotional elements of threatening stimuli, and less frequently toward negative elements [
23]. Generating non-negative interpretations requires the scanning not only of negative but also of non-negative stimuli. Due to limited attentional resources, attentional bias toward negative stimuli enhanced by cortisol elevation might hamper the allocation of attentional resources to non-negative stimuli.
Another possible mediator could be working memory impairment caused by stress-induced cortisol. It is reported that stress-induced cortisol secretion is related to working memory impairment [
24,
25]. In addition, it has been reported that the efficacy of cognitive reappraisal in the attenuation of negative affective responses is related to individual differences in working memory [
9,
26], and it is assumed that working memory would influence the generation of non-negative interpretations during cognitive reappraisal. However, whether or not working memory is related to the generation of non-negative interpretations has not been investigated. Thus, this interpretation awaits further studies.
The effects of cortisol on emotional information processing depend on the timing of its measurement after stress induction [
27]. Cortisol enhances excitability and the onset of the stress reaction from shortly after stress exposure (i.e., fast effects). These fast effects are mediated by non-genomic pathways through membrane-located receptors. Next, approximately 15–30 min after receptor activation, cortisol begins to suppress excitability and the stress reaction (i.e., slow effects). These slow effects are mediated by modification of the transcription of target genes through intracellular receptors [
28]. In line with the assumption, cortisol is associated with attentional bias toward negative stimuli when measured shortly after a stress-induction task [
3], whereas no such results were obtained when measured at longer intervals after a stress-induction task [
29]. Because the present study measured the number of non-negative interpretations generated shortly after the stress-induction task, it could capture the fast effects of cortisol to enhance emotional information processing. The generation of fewer non-negative interpretations, when measured shortly after the stress induction task in the present study, is consistent with these previous findings.
Cortisol responders had a lower baseline cortisol level and included more men. These results align with those of previous studies reporting that the basal cortisol level was negatively correlated with cortisol response [
30] and that men show higher cortisol response than women [
31,
32]. Blunted cortisol response in individuals with a higher baseline level may be due to the baseline level being close to the stress level or to a ceiling effect [
30]. Blunted response in women is presumed to be due to actions of gonadal hormones [
33]. Because responders had a lower number of post-stress non-negative interpretations with the baseline cortisol level and sex, statistically controlled, cortisol reactivity could lead to difficulty in generating non-negative interpretations. However, the baseline cortisol level and sex could impact the generation of non-negative interpretations as well as cortisol reactivity. Because individuals with a lower basal cortisol level and male sex indicate higher cortisol response, they would be likely to show changes in emotional information processing and difficulty in generating non-negative interpretations.
It is assumed that cortisol could contribute to the development and maintenance of depression [
12]. The present study suggests that higher cortisol stress reactivity or sensitivity might hamper the generation of non-negative interpretations during cognitive reappraisal, which might contribute to the maintenance of depressive symptoms.
This study has several limitations. First, the correlation between change in cortisol and change in the number of non-negative interpretations was not significant; this may be partly due to the small sample size and inadequate power to detect correlations. Second, the sex ratio was different between the responder and non-responder groups. This unbalanced sex ratio may confound the relationship between cortisol and the generation of non-negative interpretations. Third, the non-responder group showed a higher baseline cortisol level than the responder group. The higher baseline cortisol level would not be due to anticipatory anxiety because the pre-stress negative effect was not different between the groups. It has been reported that the basal cortisol level is negatively correlated to cortisol response to a stressor [
30], thus the participants with a higher basal cortisol level may have shown lower cortisol response to the relatively mild stressor used in the study.
Conclusions
The study showed that stress-induced cortisol is associated with difficulty in generating non-negative interpretations of depression-related stressful social situations. The responders generated a lower number of post-stress non-negative interpretations when sex, baseline cortisol level, and the number of pre-stress non-negative interpretations were statistically controlled. Although baseline cortisol and sex may impact the generation of non-negative interpretations as well as cortisol reactivity, the results suggest a relation between stress-induced cortisol and cognitive change, which is a later stage of cognitive emotion regulation. Although the cross-sectional study design cannot prove a causal relation, this might be caused by the cortisol acting to facilitate emotional information processing, which hampers the allocation of attentional resources to non-negative stimuli.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
HT and HS conceptualized and designed the study. HT and JS collected and analyzed the data. HT, JS, and HS interpreted the results. HT drafted the manuscript. All the authors read and approved the final manuscript.