Eye movement pattern of attention bias to emotional stimuli in women with high premenstrual symptoms
Introduction
Premenstrual syndrome (PMS) refers to a series of physiological, emotional, and behavioral symptoms among the women of reproductive age. These symptoms appear periodically in the luteal phase, with remission generally occurring within 3 days after the onset of menses, and interfere with daily functioning (Yonkers, O'Brien, & Eriksson, 2008). PMS is characterized by a combination of symptoms such as irritability, depression, anxiety, and breast tenderness (Qiao et al., 2012).
Studies have found that women with PMS have a cognitive mode of rumination (Craner, 2014; Craner, Sigmon, Martinson, & McGillicuddy, 2014; Craner, Sigmon, & Young, 2015). Rumination is a negative cognitive style, which refers to recurrent negative thinking about the causes and various possible negative consequences, without proactive problem-solving (Nolen-Hoeksema, 1991). Hunter (2003) proposed a cognitive model for women with PMS by arguing that negative cognitive appraisal of premenstrual changes may help explain the pathogenesis of PMS. Studies have shown that women with PMS reported a higher level of trait rumination than women without PMS (Craner, Sigmon, & Young, 2015), and that the level of trait rumination predicted the severity of PMS (Craner, 2014). Participants in the PMS group also showed more ruminant responses to negative emotions than those in the control group in a laboratory setting (Craner, Sigmon, & Young, 2015). The cognitive model of rumination may play an important role in elaborating the cognitive–emotional process in women with PMS (Takano & Tanno, 2008).
Recent studies found that attention biases (ABs) are associated with rumination (e.g., Armstrong &Olatunji, 2012; Kaiser et al., 2018). ABs are defined as a tendency to attend to a certain type of stimulus over others during emotional information processes (Beckwe & Deroost, 2016). ABs are driven by two components: attentional engagement and attentional disengagement (Posner, Inhoff, Friedrich, & Cohen, 1987). Attentional engagement refers to the selection and initial orientation of attention toward stimuli in the early cognitive process, whereas attentional disengagement refers to the withdrawal of attention from stimuli in the late cognitive process (Hollingworth, 2008). ABs may be caused by faster or more frequent initial orientation of attention to related stimuli, or impaired attentional disengagement. The impaired attention disengagement leads to difficulty in diverting the attention away from the related negative stimuli and in the maintenance of related positive (Clarke, MacLeod, & Guastella, 2013). In addition to the static level of attentional engagement and disengagement involved in the ABs, the dynamic processes underlying attentional engagement and disengagement are also involved in the ABs to information, manifested as returning to stimuli repeatedly (Roy-Charland, Plamondon, Homeniuk, Flesch, & Stewart, 2017).
Rumination is characterized by biased attentional processing of negative information (Owens & Gibb, 2016). For example, individuals with higher levels of trait rumination showed more ABs toward negative information (Koster, Derakshan, & Raedt, 2011). Studies have also shown that rumination and ABs are interrelated and affected by mood status such as anxiety and depression. High-anxiety individuals had stronger ABs under the condition of inducing rumination than that of inducing distraction, whereas low-anxiety individuals showed no ABs (Essmann & de Jong-Meyer, 2008). Depressed individuals with a high level of trait rumination were associated with difficulty in attentional disengagement from depression-related information (Grafton, Southworth, Watkins, & MacLeod, 2016). The difficulty of disengagement from depression-related information was found to be associated with trait rumination, but not state rumination (Donaldson, Lam, & Mathews, 2007). Armstrong and Olatunji (2012) reported that anxious individuals showed increased initial attention to threat stimuli, but no difficulty to disengage from threat stimuli. Conversely, depressed individuals did not show any increase in the initial attention to threat stimuli. Although these studies only focused on the static level of ABs, they all revealed that the affecting disorders were associated with different characteristics of altered ABs, which were closely related to rumination.
One most recent study further investigated ABs with regard to the emotional information of women with PMS (Eggert, Kleinstäuber, Hiller, & Witthöft, 2017). Researchers used the emotional Stroop paradigm with emotional words, pictures, and faces and found that participants in the PMS group had ABs toward negative emotional information. Compared to those in the control group, participants in the PMS group showed greater emotional Stroop effect to picture and facial stimuli. However, no significant difference was observed between the PMS and control groups on Stroop effects to word stimuli. With respect to the facial stimuli, researchers also found a type of paradox effect (Stroop facilitation) in the PMS group; i.e., emotional stimuli accelerated the speed of cognitive processing. An earlier study indicated that emotional Stroop tasks could not distinguish between the attentional engagement or disengagement of ABs (Jansen, Nederkoorn, & Mulkens, 2005). It is unclear whether the contradiction of the Stroop effect to different stimuli can be attributed to the acceleration of attentional engagement or the impaired attentional disengagement. Because the traditional AB paradigms heavily rely on the speculative cognitive process by measuring the reaction time; the components and the process of ABs cannot be directly observed. Additionally, it also ignores the dynamics of attentional processing involved in the ABs (Roy-Charland et al., 2017). Because eye-tracking technology has been used in the research of attentional engagement and allows for direct and continuous measurements of overt visual attention, researchers recently proposed that eye-tracking technology could provide an important supplement to reaction time measures (Armstrong, Sarawgi, & Olatunji, 2012).
Based on previous research, this study used the paired emotional picture-viewing paradigm with eye-tracking technology to examine the components, process, and dynamics of emotional information's ABs by comparing women with high premenstrual symptoms (HPMS) and women with low premenstrual symptoms (LPMS). As mentioned above, the symptoms of PMS include both depression and anxiety. Therefore, we hypothesized that the eye movement patterns in women with HPMS would be different in patients with anxiety and depression. We further hypothesized that, compared with women with LPMS, women with HPMS would have accelerated attentional engagement toward negative emotional stimuli and reduced attentional engagement in the orientation to positive stimuli in the early cognitive process. However, they would have difficulties in attentional disengagement from negative emotional stimuli and in the maintenance of positive stimuli in the late cognitive process. Moreover, women with HPMS would return their attention back to negative stimuli more frequently than those with LPMS. Besides, ABs were associated with the cognitive mode of rumination in women with HPMS. The differences in attentional patterns would occur only during the premenstrual period, not in the postmenstrual period.
Section snippets
Participants
PMS Scale (PSS; Zhao, Wang, & Qu, 1998) was used in this study for sample selection through posters or online advertisements. According to the clinical cutoffs of PSS, those with scores higher than 10 (i.e., moderate or severe symptoms) were divided into the HPMS group, and those with scores lower than 6 (i.e., no symptoms) were divided into the LPMS group. In addition, all participants were required not to have any of the following situation: pregnancy, breastfeeding, current use of hormonal
Hormone level results
The salivary estradiol and progesterone levels in the two groups are shown in Table 2, and the details of results are presented in Supplementary Materials. The results are consistent with the description of hormonal changes in the menstrual cycle (Wactawski-Wende et al., 2010), indicating that the test time of the two groups satisfies the experimental requirements.
Questionnaire results
The questionnaire results show that the scores on the PSS of the HPMS group (15.16 ± 3.75) are significantly higher than those of
Discussion
This study used a free viewing paradigm combined with eye-tracking technology and self-reporting questionnaires to examine the differences in the ABs to emotional information and cognitive characteristics between women with HPMS and women with LPMS. It was found that the HPMS and LPMS groups showed different eye movement patterns of ABs to different emotional information. In the attentional engagement of early cognitive processing, participants in the HPMS group had a biased orientation toward
Contribution of the individual authors
Lirong Chen:Conceptualization, Methodology, Software, Formal analysis, Writing - Original Draft. Lulu Hou:Investigation.Renlai Zhou:Conceptualization, Methodology, Writing - Review & Editing, Supervision, Funding acquisition.
Role of funding source
This work was supported by Nanjing Institute of Minor Mental Health Research [grant number 2020ZK-ZK05] and Fundamental Research Funds for the Central Universities [grant number 2020300048].
Declaration of competing interest
The authors declare that they have no conflict of interest.
Acknowledgements
We are grateful to Dr Jiang Da, who is working at the Department of Psychology of Education University of Hong Kong and Professor Hu Senqi, who is working at the Department of Psychology of California State University Los Angelesd, They provided valuable comments and suggestions for our revised manuscript.
References (48)
- et al.
Hormonal cycles, brain network connectivity, and windows of vulnerability to affective disorder
Trends in Neurosciences
(2018) - et al.
Eye tracking of attention in the affective disorders: A meta-analytic review and synthesis
Clinical Psychology Review
(2012) - et al.
Orienting and maintenance of gaze in contamination fear: Biases for disgust and fear cues
Behaviour Research and Therapy
(2010) - et al.
Pain-related attentional processes: A systematic review of eye-tracking research
Clinical Psychology Review
(2020) - et al.
Rumination and attention in major depression
Behaviour Research and Therapy
(2007) - et al.
Emotional interference and attentional processing in premenstrual syndrome
Journal of Behavior Therapy and Experimental Psychiatry
(2017) - et al.
A naturalistic visual scanning approach to assess selective attention in major depressive disorder
Psychiatry Research
(2003) - et al.
Selective visual attention for ugly and beautiful body parts in eating disorders
Behaviour Research and Therapy
(2005) - et al.
Time course of selective attention in clinically depressed young adults: An eye tracking study
Behaviour Research and Therapy
(2008) - et al.
Understanding depressive rumination from a cognitive science perspective: The impaired disengagement hypothesis
Clinical Psychology Review
(2011)
Why are women so vulnerable to anxiety, trauma-related and stress-related disorders? The potential role of sex hormones
Lancet Psychiatry
Prevalence of premenstrual syndrome and premenstrual dysphoric disorder in a population-based sample in China
European Journal of Obstetrics & Gynecology and Reproductive Biology
Premenstrual syndrome
The Lancet
Attentional bias toward threat in contamination fear: Overt components and behavioral correlates
Journal of Abnormal Psychology
Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study
Psychological Bulletin
Attentional biases in ruminators and worriers
Psychological Research-Psychologische Forchung
Biases in visual orienting to negative and positive scenes in dysphoria: An eye movement study
Journal of Abnormal Psychology
Assessing the role of spatial engagement and disengagement of attention in anxiety-linked attentional bias: A critique of current paradigms and suggestions for future research directions
Anxiety, Stress & Coping
Statistical power analysis for the behavioral Sciences
An investigation of the relationship between self-focused attention and premenstrual symptoms
Self-focused attention in response to laboratory stressors among women with premenstrual disorders
Archives of Women's Mental Health
Premenstrual disorders and rumination
Journal of Clinical Psychology
Self-focused attention and symptoms across menstrual cycle phases in women with and without premenstrual disorders
Cognitive Therapy and Research
Ruminative minds, wandering minds: Effects of rumination and mind wandering on lexical associations, pitch imitation and eye behaviour
PloS One
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2022, International Journal of PsychophysiologyCitation Excerpt :It was found that the PMSS scores of the PMS group (via prospective measurement) were higher than that of the non-PMS group (p < .001). Therefore, it has been effectively and widely used to measure the severity of PMS in previous studies (Chen et al., 2022; Deng et al., 2019; Hou et al., 2021). The CERQ (Garnefski et al., 2001), which was translated into Chinese (Zhu et al., 2007), was used to measure the participants' emotion regulation.