Attention as a central mechanism of socioemotional development
By Koraly Pérez-Edgar
Koraly Pérez-Edgar is an associate professor of psychology at The Pennsylvania State University, where she leads the Cognition, Affect, and Temperament (CAT) Lab. Pérez-Edgar received an AB from Dartmouth College, an MA and PhD from Harvard University, and postdoctoral training at the University of Maryland and NIMH. Before joining the faculty at Penn State, she was an assistant professor of psychology at George Mason University. The CAT Lab examines the roles that temperament and attention play in socioemotional development. The lab uses multiple methods — questionnaires, behavioral observations, computer-based tasks, psychophysiology and neuroimaging. Pérez-Edgar’s work has been funded by numerous sources, including an NIMH K01 Career Development Award, a NARSAD Young Investigator Award, and an NIMH Biobehavioral Research Award for Innovative New Scientists (BRAINS). Author website.
Developmental Tethers Link Childhood Traits to Adult Outcomes
Developmental psychology has focused on mechanisms, both external and internal to the child, that shape, refine, and reinforce patterns of development over time. Developmental trajectories are the pathways children take from infancy (with all of the promise and risk that it holds) into adulthood and beyond. For most children, these trajectories travel through a happy medium, producing adolescents and young adults who can flexibly adapt to their environments and lead successful, independent lives. Even when examining young children who appear at elevated risk for maladaptation, the same positive trajectory holds true for the majority of children (Degnan & Fox, 2007). For example, even among very shy children, the majority do not go on to have social anxiety disorder. This pattern may act as the developmental equivalent of the statistical construct of regression to the mean. Over the course of time, development appears to smooth away the jagged edges of early risk through naturally occurring maturational, experiential, and social processes.
However, for a subset of children the risks evident early in life persist, calcifying into a pattern of maladaptation through childhood and into adulthood. Since children appear to be more open to prevention and intervention (Pine, Helfinstein, Bar-Haim, Nelson, & Fox, 2009), over time it becomes increasingly more difficult to redirect maladaptive trajectories. Thus it is exceedingly important to identify and target the mechanisms at play early in life. These mechanisms — developmental tethers — bind children to specific trajectories and resist the normal ameliorative or “smoothing away” process. From our lab’s perspective, developmental tethers grow out the child’s individual early traits or biases. These biases provoke an environmental response. The child processes and interprets these responses and frames subsequent behaviors based on the conclusions drawn. This can become cyclical, growing progressively more entrenched (and biased) with each successive iteration.
Our work has focused on attention as one such tether, specifically examining the role attention biases to threat may play in increasing risk for anxiety, particularly in children with extreme temperamental traits (Pérez-Edgar & Fox, 2005). We focus on behavioral inhibition, a trait that is rooted in biology, is evident in the first year of life, and is associated with up to a four-fold increase in risk for clinical anxiety by adolescence (Chronis-Tuscano et al., 2009). This work takes advantage of neuroscience research that has carefully plotted the neural structures that support attention and emotion (Nelson & Guyer, 2011; Nelson, Leibenluft, McClure, & Pine, 2005), coupled with our knowledge of how developmental processes unfold over time (Fox & Pine, 2012). As a result, we are now in a position to identify and target discrete brain-based attention mechanisms for intervention that may prove to be efficient, effective, and widely disseminable supplements to traditional forms of treatment, such as cognitive behavioral therapy (CBT).
Attention Is a Central Guide to the Child’s Environment
From birth, individuals are bombarded with more sensory stimuli than one could ever hope to process and respond to. As such, we must learn to selectively attend to those aspects of the environment that support our current goals. At the same time, however, we must also remain open to unexpected, yet salient, events that can (and, perhaps, even should) disrupt our current plans. The famed neuroscientist Joseph LeDoux (1994) formulated the iconic example of the hiker moving through the forest who must closely attend to the path’s route while also noting the unexpected and unwanted appearance of snakes. This delicate balancing act requires sophisticated neural systems that can monitor and direct flexible, goal-directed behavior (Ridderinkhof, van den Wildengberg, Segalowitz, & Carter, 2004).
This balancing act of attending to goals while responding to unexpected information is strongly rooted in neural development and emerges slowly over time. For example, under the right circumstances young infants are captured by salient stimuli in their visual world. This can be seen when infants fixate on a toy hanging over head from a mobile. Once captured, the infant may be incapable of disengaging and looking way — leading to a great deal of frustration. This phenomena, known as “sticky fixation”, begins to dissipate at approximately three to four months of age, with the maturation of the superior colliculus — a small region nestled in the midbrain (Johnson, 1994).
Over the course of early childhood, increasingly more sophisticated systems come on line so that the child is no longer beholden to external forces (exogenous control) and can now willfully direct his or her attention (endogenous control). This is an exceedingly complex relation, instantiated in rich neural interconnections across multiple brain regions.
As a result, we often focus on a subset of this network that we believe most clearly reflects a specific component of the link between attention and socioemotional development. For example, the anterior cingulate cortex (ACC) subserves cognitive control functions associated with monitoring the effectiveness, efficiency, and meaning of behavior and performance. The ACC is considered a transition zone between the limbic and frontal cortex (Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004), linking together the emotional processing of objects and events (rooted in the limbic system) with top-down control mechanisms (often localized to the frontal cortex).
When examining attention biases to threat and the emergence of anxiety, the focus is often on the amygdala and the ventrolateral prefrontal cortex (vlPFC). We view the amygdala as a structure centrally involved in salience detection and stimulus-reinforcement learning. The vlPFC is thought to adjust goal-directed behavior based on threat-salience information. Differences in amygdala and vlPFC activity thereby reflect both the level of threat perceived during specific events as well as the cognitive demands of the activity at hand (Bishop, 2009). However, before this interplay can take place, attention acts as a gate keeper — determining which events are allowed to “enter” this network.
Information processing models (Crick & Dodge, 1994) lay out the means by which children take in, interpret, and respond to their environment. Children must first encode a small subset of the myriad of incoming cues. They then interpret these cues, often in light of how they guide or clarify goal selection. Finally, potential responses are generated, one is chosen, and the choice is then enacted. Serving as the ‘database’ for this progression is a store of memories, social knowledge, acquired rules governing behaviors, and past emotional experiences. A simplified illustration of Crick and Dodge’s model can be found in Figure 1. One can envision a young child entering the loud and boisterous school playground with these small processing units rotating sight unseen in the mind. He must pick out from the din of voices the location and identity of potential playmates (cue encoding). From among the multiple groups, he must choose which one to approach. If he is smart, he will avoid the bullying group that teased him last week (cue interpretation based on current goals and past events) and instead approach the small group with a like-minded interest in trucks and cars (choice selection and enactment).
Figure 1. This modified representation of Crick and Dodge’s (1994) social information processing model depicts the steps by which individuals encode, process, and act on information from the environment. In this figure I have added an additional point representing attention’s role as a filter, allowing in only a subset of cues.
To the model in Figure 1, I have added a small circle representing attention in its gate-keeping role. Attention acts as a filter allowing only a small subset of potential cues into the system. Without this filter, the system would almost immediately become overwhelmed and collapse. It is the small frightened child frozen in place by the crushing, indistinguishable buzz of the school playground. As noted above, a nimble attentional filter ensures that the system remains flexible — remaining on target to reach set goals and blocking out distracters, while still able to respond to important unexpected events. This is LeDoux’s snake in the path or our small child’s bully in the playground. The danger comes when the attentional filter is biased — seeing more snakes or bullies than may actually exist.
Attention Biases and the Link to Anxiety
An exciting new area of research suggests that in anxious adults the balance of activity within the fronto-limbic network may be shifted, preferentially responding to threat-related events (Bishop, 2009; Bishop, Duncan, Brett, & Lawrence, 2004). Due to this shift, or bias, in the filter, anxious individuals detect threat in their environment more often, and at lower levels of intensity, than do their non-anxious counterparts. Anxious adults then respond in the most logical manner by retreating from the threat and avoiding in the future any situations in which they may once again encounter this threat. Unfortunately, when attention biases to threat are exceedingly high, the individual’s social world can shrink and become distorted, leading to maladaptive behaviors, social withdrawal, and, in some cases, clinical levels of anxiety.
Thus, attention mechanisms may play a pivotal role in shaping the individual’s experienced environment from the first days of life. If this view is correct, early life individual differences in attention should be associated with diverging trajectories of socioemotional development during early childhood — potentially extending into adolescence. This process may be most acute in children at risk for anxiety. Much of the focus has been on children at risk due to the temperamental trait of behavioral inhibition.
Kagan and colleagues (Garcia Coll, Kagan, & Reznick, 1984; Kagan, Reznick, Clarke, Snidman, & Garcia-Coll, 1984) were the first to describe behavioral inhibition as a salient temperamental type. Behavioral inhibition is the tendency to display signs of fear and wariness in response to unfamiliar stimuli (L. A. Schmidt et al., 1997) and this trait is marked by heightened vigilance, motor quieting, and withdrawal from novelty (Garcia Coll et al., 1984; Kagan, Reznick, & Snidman, 1987). As behaviorally inhibited children mature, they increasingly fear social circumstances, displaying poorly regulated social behavior and increased social reticence (Coplan, Rubin, Fox, Calkins, & Stewart, 1994; Fox et al., 1995). This, in turn, leads to peer rejection, low self-esteem, and poor social competence (Rubin, Chen, & Hymel, 1993; L. A. Schmidt, Fox, Schulkin, & Gold, 1999). In prospective research, behavioral inhibition emerges as one of the strongest predictors of risk for later anxiety (Chronis-Tuscano et al., 2009; Schwartz, Snidman, & Kagan, 1999).
Behavioral inhibition and anxiety share important similarities at the behavioral level, such as hypervigilance toward threat and a tendency to avoid social stressors (Fox, Henderson, Marshall, Nichols, & Ghera, 2005; Pine, 1999). They also share similar biological antecedents (Fox & Reeb-Sutherland, 2010; Pérez-Edgar & Fox, 2005). Kagan (Kagan, Reznick, & Gibbons, 1989; Schwartz, Wright, Shin, Kagan, & Rauch, 2003) has argued that behaviorally inhibited children have a lowered threshold for amygdala arousal when faced with novelty. This limbic hyperarousal impacts subsequent neural processes and, in turn, shapes social behavior.
As a first examination of attention as a developmental tether (Pérez-Edgar, McDermott, et al., 2010), my colleagues and I characterized infants at 9-months of age for high or low levels of sustained attention. We then observed trajectories of behavioral inhibition through age 7 years and social discomfort at age 14 years. We found that children with low levels of sustained attention showed increasing levels of behavioral inhibition over childhood. In addition, initial behavioral inhibition predicted adolescent functioning only in the children with low levels of sustained attention. The observed developmental trajectories may be a reflection of the important gatekeeper role that attention plays in day-to-day psychological processes, influencing the initiation, deployment, and termination of a wide range of behavior and neural functions.
Given this initial empirical foundation, we then looked to see if children with a history of behavioral inhibition also display attention biases to threat. In doing so, we carried out a series of studies using the standard task employed to quantify attention biases in anxious adults. In a dot-probe task (MacLeod, Mathews, & Tata, 1986; Mogg & Bradley, 1999), two visual stimuli, one threat-related and one neutral, are shown briefly on each trial, and their removal is followed by a small probe in the location just occupied by one of the stimuli. Participants are required to respond as fast as possible to the probe Attention bias towards threat is revealed when participants are faster to respond to probes that replace threat-related rather than neutral stimuli. Recent work has found consistent patterns of bias to threat in anxious children and adults (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van IJzendoorn, 2007; Fox & Pine, 2012). In addition, testing within the fMRI environment has also shown disturbances in both frontal (i.e., vlPFC) and limbic (i.e., amygdala) regions (Monk et al., 2006; Monk et al., 2008) in clinically anxious adolescents.
My colleagues and I presented a standard dot probe task to adolescents who had been followed since infancy and who were characterized with regard to behavioral inhibition (Pérez-Edgar, Bar-Haim, et al., 2010). We found that these adolescents showed a significant bias towards threat. Pointing to attention’s role as a developmental tether, early behavioral inhibition predicted levels of social withdrawal in adolescence only for those participants who displayed a bias toward threat. In a follow-up study with an independent cohort of young children (age 5 years), we again found that early behavioral inhibition only predicted later social maladjustment in the presence of attention biases to threat (Pérez-Edgar et al., 2011). Importantly, these data suggest that the relations between attention and social development are evident, and remarkably similar in form, both before and after the expected developmental window for the emergence of anxiety (Beesdo et al., 2007). These data also point to the role that early attention mechanisms may play in shaping broad patterns of functioning by acting as a tether between early temperamental biases and subsequent social outcomes.
Attention as a Target for Intervention for Anxiety
Building on these findings a number of laboratories are now examining attention as a direct target of intervention for anxiety (Bar-Haim, 2010). This view treats attention bias as a causal mechanism of anxiety and not simply a symptom of the disorder. If proven effective, this new line of research may greatly enhance our ability to influence the information processing biases at the heart of anxiety.
A great deal of research has examined mechanisms traditionally thought to shape developmental trajectories, such as parenting, social environment, and genetic predisposition. These studies have greatly improved our understanding of developmental risk and will help us identify those children most vulnerable to anxiety. However, they do not always provide a clear or simple path for intervention.
For example, while we know that parenting style plays an important role in ameliorating or exacerbating early temperamental biases (Williams et al., 2009), designing, implementing, and assessing effective parenting interventions is exceedingly difficult and costly. Even applying gold-standard evidence-based interventions such as cognitive-behavior therapy (CBT) face difficulties as they rely on highly trained practitioners and must be tailored for use with young children. Indeed, remission rates with first-line treatments hover at only 50% (Cartwright-Hatton, Roberts, Chitsabesan, Fothergill, & Harrington, 2004). Thus, the challenge is to identify an intervention that can effectively target individuals vulnerable to anxiety, is amenable to use with even young children, and can be widely implemented.
Recent work has therefore focused on attention bias modification (ABM) as a new mechanism for intervention. In ABM protocols employing the dot-probe task, the target location is systematically manipulated so that the targets always appear at the location opposite the threat cue. Since attending to systematic contingencies can assist in task performance, an implicitly learned bias away from the threat cue is gradually induced. MacLeod and Hagan (1992) provided initial suggestive evidence for causality, and a series of other studies extend this evidence (Bar-Haim, 2010; Hakamata et al., 2010). The results show promise: in a small study Schmidt et al (N. Schmidt, Richey, Buckner, & Timpano, 2009) found that after training, 72% of patients in the active treatment condition, relative to 11% of patients in the placebo, no longer met DSM-IV criteria for Social Anxiety Disorder (SAD). Recent work has found promising results in clinically anxious children (Bar-Haim, Morag, & Glickman, 2012; Eldar et al., 2012).
Work with ABM is in its infancy and many deep questions remain. These include: What processes are affected by ABM? How do these processes influence the deep-seated behavioral patterns seen in anxiety? How long do the effects of ABM persist? Can ABM be used effectively as a preventive tool? Finally, how do ABM-linked effects interact with the normative developmental trajectories of attention? My laboratory is one of many now working to address these questions. Indeed, our current NIMH-funded study is examining the impact of ABM on social behavior, anxious symptoms, and the neural correlates of attention in children at temperamental risk for anxiety.
Systematic research on ABM protocols are only now emerging. owever, if proven effective ABM holds the promise of a portable, efficient, easily-implemented intervention that can be used with very young children. This would increase our ability to ameliorate suffering and broaden access to treatment across geographic location, socioeconomic status, and age. Initial proof of concept studies, like the one we are carrying out, are crucial for merging theoretical promise with actual empirical data.
The work summarized here is dependent on the continued support of families who take time from their busy schedules to participate in research studies. My research has been guided by my colleagues Nathan A. Fox, Daniel S. Pine, and Yair Bar-Haim and carried out by the wonderful members of the CAT Lab. Funding support in writing this brief was provided by an NIMH BRAINS award (R01 MH094633-01).
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