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Biological Psychology 122 (2017) 110–120 Contents lists available at ScienceDirect Biological Psychology jo urnal homepage: www.elsevier.com/locate/biopsycho The beneficial effects of a positive attention bias amongst children with a history of psychosocial deprivation a,∗ b h Sonya Troller-Renfree , Katie A. McLaughlin , Margaret A. Sheridan , c,d,e,f g a Charles A. Nelson , Charles H. Zeanah , Nathan A. Fox a Department of Human Development and Quantitative Methodology, University of Maryland, College Park, United States b Department of Psychology, University of Washington, Seattle, United States c Harvard Medical School, United States d Boston Children’s Hospital, United States e Harvard Center on the Developing Child, United States f Harvard Graduate School of Education, United States g Tulane University School of Medicine, New Orleans, United States h Department of Psychology and Neuroscience, University of North Carolina, Chapel Hill, United States a r t i c l e i n f o a b s t r a c t Article history: Children raised in institutions experience psychosocial deprivation that has detrimental influences on Received 30 June 2015 attention and mental health. The current study examined patterns of attention biases in children from Received in revised form 23 March 2016 institutions who were randomized at approximately 21.6 months to receive either a high-quality foster Accepted 14 April 2016 care intervention or care-as-usual. At age 12, children performed a dot-probe task and indices of attention Available online 21 April 2016 bias were calculated. Additionally, children completed a social stress paradigm and cortisol reactivity was computed. Children randomized into foster care (N = 40) exhibited an attention bias toward positive Keywords: stimuli but not threat, whereas children who received care-as-usual (N = 40) and a never-institutionalized Attention bias Institutionalization comparison group (N = 47) showed no bias. Stability of foster care placement was related to positive bias, while instability of foster care placement was related to threat bias. The magnitude of the positive bias Psychiatric risk Social behavior was associated with fewer internalizing problems and better coping mechanisms. Within the foster care Cortisol reactivity group, positive attention bias was related to less blunted cortisol reactivity. Early adversity © 2016 Elsevier B.V. All rights reserved. Internalizing behaviors 1. Introduction the mechanisms underlying these outcomes. One hypothesized mechanism is visual attention biases (Troller-Renfree, McDermott, Children abandoned and raised in institutional care expe- Nelson, Zeanah, & Fox, 2015). Visual attention biases act as “gate rience severe psychosocial deprivation that is associated with keepers,” influencing which aspects of the environment enter and increased risk for negative outcomes across physical, neurobi- are processed by the visual stream (Pérez-Edgar et al., 2011). Visual ological, social, cognitive, emotional, and behavioral domains attention biases are commonly measured by assessing where an (Bakermans-Kranenburg, van Ijzendoorn, & Juffer, 2008; Nelson, individual instantaneously and preferentially allocates attention in Fox, & Zeanah, 2014). These adverse outcomes are thought to be the environment. By understanding what stimuli are entering the related to a lack of sensitive, contingent caregiving and absence of visual stream, we may better understand how children encode and an “expectable” environment (Nelson, 2015; Nelson et al., 2007). interact with their social world. Studies have shown that atten- Given that both cognition and social functioning are influenced tion biases are useful cognitive endophenotypes that are linked by institutional care (Colvert et al., 2008; Pollak et al., 2010; Reeb, to personality traits, resilience, and vulnerability to psychopathol- Fox, Nelson, & Zeanah, 2009), it is of great interest to identify ogy (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van Ijzendoorn, 2007; Fox, Ridgewell, & Ashwin, 2009). Two primary patterns of attention biases have been studied: ∗ threat biases and positive biases. Each has been linked to a dis- Corresponding author at: Department of Human Development and Quantita- tive Methodology, University of Maryland, 3304 Benjami Building,College Park, MD tinct constellation of social and emotional processing. Individuals 20742, United States. who exhibit an attention bias to threat—reflected in faster reaction E-mail address: [email protected] (S. Troller-Renfree). http://dx.doi.org/10.1016/j.biopsycho.2016.04.008 0301-0511/© 2016 Elsevier B.V. All rights reserved. S. Troller-Renfree et al. / Biological Psychology 122 (2017) 110–120 111 times to an angry vs. neutral facial expression—exhibit higher lev- presence of bias at a single point in time. In addition to examining els of anxiety symptoms (Vasey, El-Hag, & Daleiden, 1996), social the relations between attention biases and psychosocial outcomes avoidance (Mogg, Philippot, & Bradley, 2004) and poor emotion at age 12, we also investigated whether stability of attention biases regulation skills (Cisler & Koster, 2010) when compared to those across time were associated with other key social, emotional, and without an attention bias to threat. In contrast, a bias toward posi- physiological outcomes in previously institutionalized children. tive stimuli—reflected in faster reaction times to a happy vs. neutral Of additional interest is whether attention biases in previously facial expression—is associated with increased reward sensitivity institutionalized children are accompanied by a distinct physiolog- (Grafton, Ang, & MacLeod, 2012), positive affect (Grafton et al., ical profile. Past work has suggested that attention biases may be 2012; Troller-Renfree et al., 2015), prosocial behavior (Derryberry linked to distinct patterns of arousal and patterns of physiological & Reed, 1994; Troller-Renfree et al., 2015), approach behavior reactivity to stress (Fox et al., 2009; MacLeod, Rutherford, Campbell, (Frewen, Dozois, Joanisse, & Neufeld, 2008), adaptive emotion reg- Ebsworthy, & Holker, 2002). For instance, induced biases towards ulation skills (Joormann & Gotlib, 2007), reduced internalizing negative information appear to increase arousal, while induced symptoms (McCabe & Gotlib, 1995), and lower rates of anxiety biases away from negative information appear to buffer against (Frewen et al., 2008). stress-induced arousal (Mathews & MacLeod, 2002). Early life stress Prior research on attention biases in previously institutionalized has also been shown to negatively impact physiological reactivity children who were 8 years of age revealed that children who were to stress in both animals and humans (Gunnar, Frenn, Wewerka, & randomized to be removed from institutional care and placed into Van Ryzin, 2009; Kessler, Chiu, Demler, & Walters, 2005; Liu et al., a high-quality foster care intervention had a significantly larger 1997; McLaughlin et al., 2015; Meyer, Novak, Bowman, & Harlow, attention bias towards positive stimuli as compared to children 1975). Specifically, previously institutionalized children tend to randomized to remain in institutional care (Troller-Renfree et al., show blunted or less reactive stress reactivity (Gunnar & Vazquez, 2015). The magnitude of the positive bias was related to a num- 2001; McLaughlin et al., 2015). Blunted profiles of stress reactiv- ber of adaptive outcomes including better social engagement, more ity have been related to a myriad of negative physical and mental prosocial behavior, fewer signs of externalizing behavior problems, health outcomes such as immunosuppression, poor mental health, and less emotionally withdrawn behavior. Additionally, children risk for alcoholism, poor antibody response, autoimmune diseases, who were randomized to remain in institutional care exhibited an obesity, and poor emotional regulation (Carroll, Phillips, & Lovallo, attention bias towards threatening stimuli. These findings provide 2012; Jansen et al., 1998; Lovallo, 2011; Segerstrom & Miller, 2004). preliminary evidence for the role of the early caregiving environ- Furthermore, there is evidence suggesting that stress-induced cor- ment in shaping patterns of attention biases towards valenced tisol reactivity is associated with selective attention to emotional stimuli. However, much is still unknown about the lasting effects of stimuli (Ellenbogen, Schwartzman, Stewart, & Walker, 2002). A early environment on attention biases, and their associations with study by Ellenbogen and colleagues (2002) demonstrated that par- other developmental outcomes. ticipants who were exposed to an aversive stressor (repeatedly While only one study has formally examined the effects of losing a game against a confederate) elicited a rapid disengage- early institutionalization and intervention on attention biases, ment of attention from negatively valenced words (as measured there is evidence suggesting that psychosocial deprivation may by a spatial cuing task). These shifts of attention away from neg- disrupt certain aspects of emotion processing. Wismer Fries and ative stimuli were associated with increased negative affect and Pollak (2004) reported that internationally adopted children who lower cortisol levels during the recovery phase of the experiment, spent some portion of their early years in an institution had suggesting that disengagement from negative stimuli affect may deficits in identifying facial expressions as well as matching regulate emotional and physiological