See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/325874239 The optimistic brain: Trait optimism mediates the influence of resting-state brain activity and connectivity on anxiety in late adolescence Article in Human Brain Mapping · June 2018 DOI: 10.1002/hbm.24222 CITATIONS READS 0 116 8 authors, including: Song Wang Xun Yang Sichuan University Xi'an Thermal Power Research Institute 16 PUBLICATIONS 72 CITATIONS 38 PUBLICATIONS 316 CITATIONS SEE PROFILE SEE PROFILE Taolin Chen Xueling Suo Sichuan University Sichuan University 49 PUBLICATIONS 193 CITATIONS 18 PUBLICATIONS 60 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: first episode psychosis View project A comprehensive clinical study about patching after strabismus surgery View project All content following this page was uploaded by Song Wang on 25 June 2018. 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Received: 29 January 2018 | Revised: 3 May 2018 | Accepted: 9 May 2018 DOI: 10.1002/hbm.24222 RESEARCH ARTICLE The optimistic brain: Trait optimism mediates the influence of resting-state brain activity and connectivity on anxiety in late adolescence Song Wang1,2 | Yajun Zhao3 | Bochao Cheng4 | Xiuli Wang2 | Xun Yang3 | Taolin Chen1 | Xueling Suo1 | Qiyong Gong1,2,5 1Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital of Sichuan University, Chengdu, 610041, China 2Department of Psychoradiology, Chengdu Mental Health Center, Chengdu, 610036, China 3School of Sociology and Psychology, Southwest Minzu University, Chengdu, 610041, China 4Department of Radiology, West China Second University Hospital of Sichuan University, Chengdu, 610041, China 5Department of Psychology, School of Public Administration, Sichuan University, Chengdu, 610065, China Correspondence: Qiyong Gong, Huaxi MR Research Center (HMRRC), Department of Abstract Radiology, West China Hospital of Sichuan As a hot research topic in the field of psychology and psychiatry, trait optimism reflects the tend- University, No. 37 Guo Xue Xiang, ency to expect positive outcomes in the future. Consistent evidence has demonstrated the role of Chengdu 610041, China. trait optimism in reducing anxiety among different populations. However, less is known about the Email: [email protected] neural bases of trait optimism and the underlying mechanisms for how trait optimism protects Funding information against anxiety in the healthy brain. In this investigation, we examined these issues in 231 healthy American CMB Distinguished Professorship adolescent students by assessing resting-state brain activity (i.e., fractional amplitude of low- Award of USA, Grant/Award Number: frequency fluctuations, fALFF) and connectivity (i.e., resting-state functional connectivity, RSFC). F510000/G16916411; Changjiang Scholar Professorship Award of China, Grant/ Whole-brain correlation analyses revealed that higher levels of trait optimism were linked with Award Number: T2014190; Program for decreased fALFF in the right orbitofrontal cortex (OFC) and increased RSFC between the right Changjiang Scholars and Innovative OFC and left supplementary motor cortex (SMC). Mediation analyses further showed that trait Research Team in University of China, optimism mediated the influence of the right OFC activity and the OFC-SMC connectivity on anxi- Grant/Award Number: IRT16R52; National Key Technologies R&D Program of China, ety. Our results remained significant even after excluding the impact of head motion, positive and Grant/Award Number: 2012BAI01B03; negative affect and depression. Taken together, this study reveals that fALFF and RSFC are func- National Natural Science Foundation of tional neural markers of trait optimism and provides a brain-personality-symptom pathway for China, Grant/Award Numbers: 81621003 protection against anxiety in which fALFF and RSFC affect anxiety through trait optimism. KEYWORDS: anxiety, depression, optimism, orbitofrontal cortex, psychoradiology 1 | INTRODUCTION and more investigators have looked to find positive individual traits that protect against anxiety (Duckworth, Steen, & Seligman, 2005; Park, & Anxiety is a common negative state occurring in our daily lives. It reflects a Peterson, 2009). As one of these character strengths, trait optimism refers complex cognitive and affective change in response to potential threats in to an individual’s general expectation regarding future positive outcomes thefuture(Grupe,&Nitschke,2013).Giventheroleofanxietyinthe (Carver, & Scheier, 2014; Carver, Scheier, & Segerstrom, 2010). Converg- development of physical illnesses and psychiatric disorders (Bower et al., ing evidence has indicated that trait optimism plays an essential role in an 2010; Brown, Chorpita, & Barlow, 1998; Rawson, Bloomer, & Kendall, individual’s physical and mental health (Alarcon, Bowling, & Khazon, 2013; 1994; Zinbarg, & Barlow, 1996), exploring factors for reducing anxiety is Andersson, 1996). In particular, trait optimism is related to engagement one main goal in the field of psychology, psychiatry and psychoradiology. coping, emotional regulation and resilience against stressful life events With the success of positive psychology over the past two decades, more (Carver et al., 2014; Carver et al., 2010; Nes, & Segerstrom, 2006; Wu Hum Brain Mapp.2018;1–13. wileyonlinelibrary.com/journal/hbm VC 2018 Wiley Periodicals, Inc. | 1 2 | WANG ET AL. et al., 2013). These psychological constructs have been found to be the This measure has been widely used to investigate the neural correlates crucial prerequisites for reducing anxiety (Cisler, Olatunji, Feldner, & For- of human personality traits (e.g., Kong et al., 2017; Kong et al., 2015; syth, 2010; Hjemdal et al., 2011; Kennedy, Duff, Evans, & Beedie, 2003; Kunisato et al., 2011; Wang et al., 2017b; Wang et al., 2017d). As Ng, Ang, & Ho, 2012). Evidence from numerous empirical investigations another popular measure for low-frequency fluctuations correlations, has confirmed that trait optimism can predict anxious symptoms among resting-state functional connectivity (RSFC) reflects the synchroniza- both clinical and healthy populations (e.g., Dooley, Fitzgerald, & Giollabhui, tion among different brain regions (Fox & Raichle, 2007). Increasing 2015; Griva, & Anagnostopoulos, 2010; Morton, Mergler, & Boman, evidence has suggested that RSFC is a good neural marker of personal- 2014; Rajandram et al., 2011; Schweizer, Beck-Seyffer, & Schneider, ity traits (e.g., Adelstein et al., 2011; Pan et al., 2016; Sampaio et al., 1999; Sheridan, Boman, Mergler, & Furlong, 2015; Siddique et al., 2006; 2014; Takeuchi et al., 2013; Wang et al., 2017c). In summary, fALFF Yu et al., 2015; Zenger et al., 2010). In the current study, we used resting- and RSFC are suitable for examining the neural bases of trait optimism. state functional magnetic resonance imaging (RS-fMRI) to examine the To our knowledge, only two studies have used fALFF and RSFC functional brain bases of trait optimism and then explore how trait opti- via RS-fMRI to explore the neural correlates of trait optimism. First, mism reduces anxiety in the brain. In brief, we used a multi-dimensional Wu et al. (2015) reported an association between individual differences method (i.e., a brain-personality-symptom method) to investigate the asso- in trait optimism and the fALFF in the medial PFC. However, the sam- ciations among resting-state brain activity and connectivity, trait optimism ple size of this study was quite small, and the sex ratio was dispropor- and anxiety in a large sample of healthy adolescent students (N 5 231). tionate (46 female and 4 male). Moreover, the statistical analyses were Although the protective effect of trait optimism on anxiety has been conducted for a given mask including several brain regions but not for established, the neural bases of trait optimism are not fully understood. the whole-brain mask. These limitations might limit the generalizability Evidence from the limited literature has suggested that the function and of their findings. Second, through an analysis of RSFC, Ran et al. (2017) structure of the prefrontal cortex (PFC) are crucial for trait optimism observed that individual differences in trait optimism were correlated (Beer & Hughes, 2010; Dolcos et al., 2016; Grimm et al., 2009; Moran with the RSFC between the ventral medial PFC and inferior frontal et al., 2006; Pauly, Finkelmeyer, Schneider, & Habel, 2013; Sharot, Korn, gyrus. It is worth noting that the RSFC analysis used in this study & Dolan, 2011; Sharot, Riccardi, Raio, & Phelps, 2007). For instance, two depended on a region of interest (ROI; i.e., ventral medial PFC), which studies based on task-related fMRI reported that when participants imag- was selected from prior studies but not identified in a single cohort of ined future positive events, there was increased activity in PFC regions participants. In addition, to our knowledge, no study has investigated including the orbitofrontal cortex (OFC), the medial PFC, the superior/ the neural bases of trait optimism in young participants (e.g., adoles- inferior frontal gyrus and the anterior cingulate cortex (Sharot et al., cents). Considering that the brains of the adolescents are undergoing 2011; Sharot et al., 2007). Similarly, increased activity of PFC regions functional and structural reformation (Blakemore & Robbins, 2012; (e.g., OFC, medial PFC and anterior cingulate cortex) has