Attention bias modification in depression: A randomized trial using a novel, reward-based, eye-tracking approach
Introduction
Biased attention towards negatively-valenced information is thought to be a significant contributing factor in the development, maintenance, and recurrence of depression. Individuals with depression tend to avoid allocating attention toward positive stimuli and preferentially attend to negative stimuli (Gotlib et al., 2004; Koster et al., 2005; Joormann & Gotlib, 2007; Peckham et al., 2010, Duque & Vázquez, 2015; Lazarov et al., 2018). These patterns of attention have been associated with perseverative processing of negatively valanced information in the form of rumination, and impaired affective regulation due to difficulty disengaging from negative stimuli (Sanchez et al., 2013; Arditte & Joormann, 2014; Sanchez-Lopez et al., 2019; Yaroslavsky et al., 2019). Recent models have linked attentional disengagement and rumination, proposing that the inability to attentionally disengage from sad information promotes the maintenance of ruminative thinking (Whitmer & Gotlib, 2013; Yaroslavsky et al., 2019).
Negative biases in depression have been found to extend to other cognitive functions, such as information processing and memory (Duque & Vázquez, 2015). Compared to healthy participants, positive information is maintained for less time in working memory of depressed participants, whereas negative information is integrated faster and maintained for longer (Levens & Gotlib, 2010). Individuals with depression reliably show a bias towards the preferential processing, recall, and memory of sad information (Bradley et al., 1996; Joormann et al., 2007; Lloyd & Lishman, 1975). Thus, initial biased attention towards sad information may be compounded by difficulty disengaging from that information, ruminative thinking, and remembering more sad than happy information. Modifying initial biased attention has therefore been identified as a potential treatment focus, as early modification may be able to help prevent subsequent ruminative thought patterns and associated memory biases.
Attempts at intervention have typically focused on the use of dot-probe attention bias modification (ABM) paradigms. These procedures attempt to train attention towards positive stimuli and away from negative stimuli. In ABM, attention is diverted away from negatively valanced stimuli by preferentially placing a probe in the same location as a neutral or positive stimulus, thus influencing the focus of attention to be more frequently on the neutral or positive stimulus and less frequently on the negative stimulus (MacLeod et al., 2002). ABM paradigms show some effectiveness at decreasing attentional bias for negative information, increasing attention allocation for positive stimuli, and decreasing depressive symptoms (Wells & Beevers, 2010; Beevers et al., 2015; Li et al., 2015; Yang et al., 2015; LeMoult et al., 2016). However, the diverse methodology, stimuli, and design of ABM research has led to conflicting and inconsistent results, with other studies not significantly manipulating attention or improving mood (Kruijt et al., 2013; De Voogd et al., 2014; Everaert et al., 2015; Platt et al., 2015). Meta-analytic research has not supported the effects of dot-probe ABM for depression, finding limited evidence for symptom or mood improvements (Mogoaşe et al., 2014). The limitations of the dot-probe include its transient nature (capturing only momentary attention rather than naturalistic attention) and exclusive use of motor-based, indirect reaction time data to assess bias, which may be confounded (e.g., measuring motor impairment, processing speed, sustained attention) (Armstrong & Olatunji, 2012; Mogoaşe et al., 2014; Burris, Barry-Anwar, & Rivera, 2017). Poor internal consistency and test-retest reliability are also commonly reported (Schmuckle, 2005; Staugaard, 2009; Kappenman et al., 2014). Moreover, single-session dot-probe paradigms often fail to achieve significant effects, yet they remain common approaches (Kruijt et al., 2013; Arditte & Joormann, 2014; Everaert et al., 2015; Platt et al., 2015). The lack of positive results in such brief paradigms may be a combination of insufficient training duration and the use of unreliable paradigms such as the dot-probe (Everaert et al., 2015).
In addition to the use of the dot-probe and single-session designs, limitations in ABM research stem from the tendency to recruit either dysphoric or undergraduate populations with non-clinical levels of depressive symptoms (Ferrari et al., 2016; Möbius et al., 2018; Wells & Beevers, 2010; Yang et al., 2015). According to a meta-analysis by Armstrong and Olatunji (2012), individuals who meet the cut-off scores for major depressive disorder show more robust bias toward negative stimuli compared to those with lower or subclinical scores.
More recently, ABM studies have used eye tracking as a measure of real-time attentional biases with greater ecological validity than previous paradigms. Eye-tracking improves upon the dot-probe paradigm by providing a continuous measure of attention via eye movements, which are more proximally related to attention than manual key presses and thus may improve the efficiency of attention measurement (Arditte & Joormann, 2014; Armstrong & Olatunji, 2012). Eye-tracking paradigms have been found to have higher reliability than dot-probe measures (Wechsler, 1997a; Christiansen et al., 2015). Eye-tracking has been applied to the measurement of attentional bias through free-viewing tasks (Sanchez et al., 2013), as well as used in combination with the dot probe to determine when participants fixate on positive and negative stimuli; this ensures that attention is redirected towards positive stimuli and away from negative stimuli before a task progresses (Ferrari et al., 2016; Möbius et al., 2018). Beyond providing a more robust measure of bias, a lesser-explored application of eye-tracking is its potential as a treatment tool to directly modify biased attention. There is ample evidence to suggest that human emotional response can be modified by adapting the contingencies around a person based on their response (e.g., traditional biofeedback paradigms). More recently, different technologies (e.g., eye-tracking, fMRI) have been used to modify brain and behaviour response; for example, Young et al. (2017) found that fMRI-measured amygdala response to positive images could be modified using principles of biofeedback. A potential method for overcoming limitations of previous ABM research is to provide real-time feedback from tracking eye movements to modify the environment and shape behaviour. While the dot-probe leads to the shifting of attention as designated by the probe, eye-tracking can allow a person's initial behaviour (e.g., looking at a negative or positive stimulus) to be either reinforced or punished, ultimately shaping their behaviour through the intentional disengagement from negative stimuli and processing of positive information, rather than simply redirecting their attention. Only two studies to date have explored modifying attention in depression using eye-tracking-based feedback; Sanchez et al. (2016; Sanchez-Lopez et al., 2019) instructed participants to allocate attention to text that contained positive words, and provided feedback in the form of green or red frames surrounding positive or negative words, respectively. That study, conducted among non-clinical undergraduates, found that eye-tracking-based feedback led to more sustained attention on positive information and reductions in state rumination (Sanchez-Lopez et al., 2019). Thus, there is evidence that eye-tracking feedback can manipulate negative attention bias, but this has not yet been explored using facial affect or among depressed populations.
The effectiveness of affective ABM in depression is mixed. Few studies have addressed the aforementioned weaknesses in design and implementation to examine whether the issue is a problem of concept or execution. We aimed to examine whether ABM might be more effective in a paradigm that addresses these shortcomings.
The aim of the present proof-of-principle randomized controlled trial was to explore the effects of a novel, reward-based, free-viewing ABM paradigm on attentional bias, emotional memory, and depressive symptoms. The design of this study improves upon past research in three ways: 1) overcoming the limits of the dot-probe through a free-viewing, eye-tracking training paradigm; 2) multiple training sessions; and 3) recruiting only individuals with major depressive disorder (MDD). We hypothesized that ABM, compared to sham control, would reduce negative information bias and affect bias (i.e., memory for valenced items), and improve depressive symptoms and quality of life. Exploratory analyses examined whether trait rumination was related to training outcomes.
Section snippets
Sample
Participants were 40 adults recruited from community mental health clinics in Ontario, Canada between January 2017 and March 2018. Participants met the following criteria: a) a diagnosis of major depressive disorder, confirmed with a structured diagnostic interview (Mini International Neuropsychiatric Interview) (Sheehan et al., 1998); 2) age 18 to 65; b) normal or corrected-to-normal vision; and c) proficiency in English. Exclusion criterion was any medical illness with compromised
Active
The attention bias modification task was developed for the present study and designed to train participants’ attention away from negative stimuli and towards positive stimuli through punishment and reward, respectively.
The active training task involved the presentation of one positively and three negatively valenced faces (displaying either happiness or sadness, respectively) per trial, selected from the NimStim Set of Facial Expressions (Tottenham et al., 2009). Trials began with a black
Attentional bias1
A free-viewing attention task was used to assess affective attentional biases. In this task, two faces from the Karolinska Directed Emotional Faces database (Lundqvist et al., 1998) were presented side by side on the screen: either a happy or sad face was paired with
Sample characteristics and correlations among baseline measures
Descriptive characteristics of each group are presented in Table 1. The groups did not differ on any of the demographic or symptom measures at baseline, with the exception of sex; the sham training group had significantly fewer men. Bivariate correlations between baseline and symptom measures in the overall sample are presented in Table 2.
Primary outcome
Attentional bias. There were no significant main effects of time, F (1, 38) = 0.58, p = .45, partial η2 = 0.015, nor group, F (1, 38) = 2.34, p = .11, partial
Principal findings
Biased attention towards negative information is a well-replicated phenomenon in mood disorders, but the ability to modify this bias has had mixed success. We developed a novel paradigm to determine whether attention bias could be shaped with a reward-based eye-tracking intervention. This proof-of-principle study demonstrated the efficacy of a novel intervention using an eye-tracking attention shaping procedure to modify negative attentional biases in adults with depression, such that
CRediT authorship contribution statement
Stephanie M. Woolridge: Conceptualization, Methodology, Software, Formal analysis, Writing - original draft, Writing - review & editing, Project administration. Geoffrey W. Harrison: Conceptualization, Methodology, Software, Formal analysis, Writing - review & editing. Michael W. Best: Conceptualization, Methodology, Formal analysis, Writing - review & editing. Christopher R. Bowie: Conceptualization, Methodology, Formal analysis, Writing - review & editing, Funding acquisition, Supervision.
Declaration of competing interest
We wish to draw the attention of the Editor to the following facts which may be considered as potential conflicts of interest and to significant financial contributions to this work:
· CRB has been a consultant to Boehringer Ingelheim, Pfizer, and Lundbeck. He has grant support from Pfizer, Takeda, and Lundbeck. CRB receives in-kind research accounts from Scientific Brain Training Pro and royalties from Oxford University Press.
We confirm that the manuscript has been read and approved by all
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