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Neural Basis Underlying the Trait of Attachment Anxiety and Avoidance Revealed by the Amplitude of Low-Frequency Fluctuations An

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Neural Basis Underlying the Trait of Attachment Anxiety and Avoidance Revealed by the Amplitude of Low-Frequency Fluctuations An Deng et al. BMC Neurosci (2021) 22:11 https://doi.org/10.1186/s12868-021-00617-4 BMC Neuroscience RESEARCH ARTICLE Open Access Neural basis underlying the trait of attachment anxiety and avoidance revealed by the amplitude of low-frequency fuctuations and resting-state functional connectivity Min Deng1,2†, Xing Zhang1†, Xiaoyan Bi3 and Chunhai Gao4* Abstract Background: Attachment theory demonstrates that early attachment experience shapes internal working models with mental representations of self and close relationships, which afects personality traits and interpersonal relation- ships in adulthood. Although research has focused on brain structural and functional underpinnings to disentangle attachment styles in healthy individuals, little is known about the spontaneous brain activity associated with self- reported attachment anxiety and avoidance during the resting state. Methods: One hundred and nineteen individuals participated in the study, completing the Experience in Close Rela- tionship scale immediately after an 8-min fMRI scanning. We used the resting-state functional magnetic resonance imaging (rs-fMRI) signal of the amplitude of low-frequency fuctuation and resting-state functional connectivity to identify attachment-related regions and networks. Results: Consequently, attachment anxiety is closely associated with the amplitude of low-frequency fuctuations in the right posterior cingulate cortex, over-estimating emotional intensity and exaggerating outcomes. Moreover, the functional connectivity between the posterior cingulate cortex and fusiform gyrus increases detection ability for potential threat or separation information, facilitating behavior motivation. The attachment avoidance is positively correlated with the amplitude of low-frequency fuctuation in the bilateral lingual gyrus and right postcentral and negatively correlated with the bilateral orbital frontal cortex and inferior temporal gyrus. Functional connection with attachment avoidance contains critical nodes in the medial temporal lobe memory system, frontal-parietal network, social cognition, and default mode network necessary to deactivate the attachment system and inhibit attachment- related behavior. Conclusion and implications: These fndings clarify the amplitude of low-frequency fuctuation and resting-state functional connectivity neural signature of attachment style, associated with attachment strategies in attachment anxiety and attachment avoidance individuals. These fndings may improve our understanding of the pathophysiol- ogy of the attachment-related disorder. *Correspondence: [email protected] †Min Deng and Xing Zhang contributed equally to this work and should be considered equally as frst authors 4 Research Center of Brain and Cognitive Neuroscience, Liaoning Normal University, Dalian 116029, Liaoning Province, China Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Deng et al. BMC Neurosci (2021) 22:11 Page 2 of 12 Keywords: Attachment anxiety, Attachment avoidance, Resting-state fMRI, The amplitude of low-frequency fuctuations, Functional connectivity Background of the study in the neural mechanism for diferent attachment behav- Social bonding conveys an intention to set up correla- ior in human brain activity? How can such kinds of the tions with others, of that an ordinary and well-described method be quantifed? Social bonding is not easily meas- consequence is that individual’s attachment behavior. urable, due to it is dynamic rather than static. Recently, Early in life, newborns shape the frst dyadic relationship several neural imaging studies on attachment seem to experience with their caregivers, while unresponsive, provide the possibility to reveal the neural mechanism neglecting, abusing, and aggressive models shape an inse- underlying attachment intrinsic trait. Feldman [21] sug- cure one. Specifcally, there are mainly three attachment gested that the neural system for attachment is included styles: secure attachment, attachment anxiety (AX), and in three reward embodied simulation and metalizing sys- attachment avoidance (AV). Secure attachment repre- tems. Specifcally, to explore the neural mechanism for sents a sensitive, supportive and stable attachment pat- insecure attachment stimuli [59] proposed a functional tern, and secure attachment individuals positively seek neuroanatomical framework to distinguish AX from AV. proximity and satisfaction with their relationship. How- He indicates that the neural basis underlying the AX is ever, insecure attachment generally relates to unsatisfed, related to emotional mentalization areas such as the distressing, and aggressive relationships; for example, amygdala, insula, anterior cortex. Simultaneously, the AV attachment avoidant individuals actively avoid contact is related to cognitive control areas, including the medial with others and distance themselves from others because prefrontal cortex, precuneus, and dorsolateral prefrontal they feel more comfortable being alone and suppressing cortex. their emotions. Oppositely, attachment anxiety individ- Moreover, a multifaceted neural model of attachment ual exaggerates distress after separation and hyperac- proposes that there are potential neural processes under- tivates proximity-seeking strategy and high emotional lying attachment behavior. Brain-based study fndings expressiveness and impulsiveness (Bowlby 1969; [6, 23, revealed that attachment stimuli seem to activate emo- 31, 41], Fraley et al. 2013). tional, cognitive, and motive processing brain areas [9]. Attachment theory posits that prior experiences of As expected, both secure and insecure attachment acti- unreliable relationships can lead to defciencies in attach- vates an identical network that is primarily related to ment approach behavior [24]. Furthermore, numer- memory and emotional regulation, including the fusi- ous studies show a distinctive proximity tendency form, middle temporal, and prefrontal areas. Attachment between AX and AV. Anxiously attached people worry style has a specifc behavioral pattern that afects social about abandonment and seek support from others, but interaction and brain activation. Te hyper-activating they perceive insufcient support [8]. Tus they name strategies used by anxiously attached people mainly attachment fgures faster in lexical decision tasks [43], increase stronger emotional arousal and regulation- remember signifcant proximity-related words [42], and related areas [26]. While AV refects an inefective social show an attention bias towards threatening informa- emotion regulation, close contact with the caregiver is tion [32]. Tose avoidant attachment tendencies drive not successful in down-regulating distress [72]. Tus, the people to distance themselves from attachment fgures attachment system’s deactivation may activate emotional or thoughts. Supporting this proposal is that exposed to regulation areas and cognitive control-related areas [69]. threat avoidantly attached individuals inhibit proximity- Tere still exist specifc brain areas for insecure attach- seeking behavior, eliminate approach reaction time to ment stimuli, mainly located in the insula and parietal secure attachment pictures in the approach-avoidance area with distinctive functions on emotional arousal and task (AAT), which spends more time to judge the direc- social information [9]. tion of the picture in a picture magnifying task [66], and However, previous brain mapping reveals the difer- increase the accessibility to unfavorable attachment rel- ence between the AX and AV; it is still unclear whether evant memories [33]. these specifc neural patterns still exist under spontane- Despite previous studies addressing attachment ous brain activity? Tat is to say, are these specifc neu- behavior pattern diferences, still vital questions remain ral mechanisms induced by attachment situation or unsolved. Does the nature of the attachment behavioral attachment intrinsic traits as personality? Resting-state distinction depend on attachment-relevant context or brain mapping studies indicated that spontaneous brain attachment inner working model? Is there any diference activity exhibited individual innate characteristics [54, Deng et al. BMC Neurosci (2021) 22:11 Page 3 of 12 73]. It has many advantages in addressing the enduring attachment anxiety and avoidance [35]. Before the exper- trait’s neural correlations (Yuan et al. 2014). Several stud- iment, all participants
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