HHS Public Access Author manuscript Author Manuscript
Emotion. Author manuscript; available in PMC 2017 February 01. Published in final edited form as: Emotion. 2016 February ; 16(1): 110–116. doi:10.1037/emo0000093.
A Novel Attention Training Paradigm Based on Operant Conditioning of Eye Gaze: Preliminary Findings Rebecca B. Price1, Inez M. Greven2, Greg J. Siegle1, Ernst H.W. Koster3, and Rudi De Raedt3 1University
Author Manuscript
2Bangor 3Ghent
of Pittsburgh School of Medicine, Pittsburgh, PA
University, Bangor, UK
University, Belgium
Abstract
Author Manuscript
Inability to engage with positive stimuli is a widespread problem associated with negative mood states across many conditions, from low self-esteem to anhedonic depression. Though attention retraining procedures have shown promise as interventions in some clinical populations, novel procedures may be necessary to reliably attenuate chronic negative mood in refractory clinical populations (e.g., clinical depression) through, e.g., more active, adaptive learning processes. In addition, a focus on individual difference variables predicting intervention outcome may improve the ability to provide such targeted interventions efficiently. To provide preliminary proof-ofprinciple, we tested a novel paradigm using operant conditioning to train eye gaze patterns towards happy faces. Thirty-two healthy undergraduates were randomized to receive operant conditioning of eye gaze towards happy faces (Train-Happy) or neutral faces (Train-Neutral). At the group level, the Train-Happy condition attenuated sad mood increases following a stressful task, in comparison to Train-Neutral. In individual differences analysis, greater physiological reactivity (pupil dilation) in response to happy faces (during an emotional face-search task at baseline) predicted decreased mood reactivity following stress. Preliminary results suggest that operant conditioning of eye gaze towards happy faces buffers against stress-induced effects on mood, particularly in individuals who show sufficient baseline neural engagement with happy faces. Eye gaze patterns to emotional face arrays may have a causal relationship with mood reactivity. Personalized medicine research in depression may benefit from novel cognitive training paradigms that shape eye gaze patterns through feedback. Baseline neural function (pupil dilation) may be a key mechanism, aiding in iterative refinement of this approach.
Author Manuscript
Keywords attentional bias; attention training; eyetracking; mood; pupil
Corresponding author information: Rebecca B. Price, University of Pittsburgh School of Medicine, Pittsburgh, [email protected].
Price et al.
Page 2
Author Manuscript
Introduction
Author Manuscript
Cognitive biases away from positive information, and towards negative information, are posited to play a critical role in the etiology and maintenance of negative affective conditions (e.g., Gotlib & Joormann, 2010) by promoting hyper-awareness of negative information, limiting awareness of positive information, and reinforcing maladaptive beliefs (e.g., Clark, Beck, & Alford, 1999; de Raedt & Koster, 2010). A growing literature suggests attention retraining techniques designed to modify attentional bias can effectively reduce clinical symptoms (MacLeod & Clarke, 2015). However, while these techniques appear to have relatively robust effects on some conditions (e.g., clinical anxiety), results of extant attention retraining studies in the context of other disorders (e.g., acute depression) have been mixed (reviewed by Mogoase, David, & Koster, 2014). Novel strategies to ameliorate attentional bias may help to address this gap in the clinical applicability of attention retraining techniques and broaden the range of individuals who might receive benefit.
Author Manuscript
Here, we sought to 1) provide preliminary proof-of-principal for one such novel strategy— operant (feedback-based) conditioning of eye gaze towards happy faces—by testing its effects on mood reactivity in a healthy sample, and 2) identify individual differences in neural engagement (indexed by pupil dilation) at baseline that can predict favorable response to the strategy, as an integral step towards further intervention refinement. Several specific features of the training paradigm were selected in the hopes of maximizing translational relevance to depressive patients. Foremost was an active, adaptive, operant learning process utilizing positive feedback—an effective means of enhancing learning (Masters, Maxwell, & Eves, 2009). We also used a training goal of increased focus on positive stimuli, designed to remediate a key attentional pattern in depression (e.g., Gotlib, McLachlan, & Katz, 1988); relatively ecologically valid stimuli (arrays of twelve emotional faces)(Dandeneau & Baldwin, 2004); and on-line, continuous measurement of eye gaze patterns to provide information proximal to the modification of visual gaze itself, rather than more ambiguous and complex measures such as manual response latencies.
Author Manuscript
Even if mood improvement is observed at the group level, individual differences in neural engagement may moderate training effects (Collier & Siegle, 2015; Siegle et al., 2014), providing clues for what psychophysiological processes must be engaged to maximize benefit. Thus, the second goal of the study was to evaluate baseline neural engagement as a predictor of post-training mood reactivity, using pupil dilation as a marker of neural engagement (Beatty, 1986; Koikegami & Yoshida, 1953) during a relevant face-search task. Consistent with previous pupil findings in depression (Collier & Siegle, 2015; Siegle et al., 2014), we specifically hypothesized that greater neural engagement with training-relevant stimuli (here, happy faces; i.e., greater pupil dilation when happy faces were presented) would predict more favorable post-training mood outcomes. Incorporating neurophysiological moderator analysis from the earliest stages of intervention development strongly promotes the ability to identify key intervention targets and make iterative refinements to expand the intervention’s reach, if and when dissemination becomes warranted.
Emotion. Author manuscript; available in PMC 2017 February 01.
Price et al.
Page 3
Author Manuscript
Method Participants Thirty-two healthy undergraduates (mean=20.56y, SD=3.94; 8 male), were randomized to experimental vs. control training (n=16/group) and completed the protocol (Figure-1). The local ethics committee approved the study. Informed consent was obtained from all participants. Operant conditioning of eye movements
Author Manuscript
We trained participants to direct their attention towards a specific emotion (experimental condition: happy; control condition: neutral). Following a fixation cross (presented until 250ms gaze fixation was detected), pictures of 12 different women from the NimStim set were presented pseudo-randomly in a diamond pattern. Six different emotional expressions were displayed (happy, angry, sad, fearful, disgusted, neutral—two faces per emotion; details in Supplement). Participants were instructed to attentively observe the pictures and were told they would hear a short, positive sound after responding “correctly.” No further instructions were given. When participants fixated on the target stimulus for 250ms within the time limit, a short sound designated correct completion. Otherwise, the trial ended and the experiment continued without feedback.
Author Manuscript
Participants were presented with at least 4 blocks of 36 trials. The first block began with a trial time limit of 3000ms. Continuation to faster blocks was adaptively based on performance. If 80% or more of trials were completed correctly, the time limit was decreased by 500ms (until the last block, which had a 1000ms limit). Otherwise, that speed was repeated. The experiment automatically stopped after the same speed was repeated 3 times (4 times for the initial block). Behavioral outcomes of training Training success was assessed using data from each participant’s first and last block. The primary outcome was latency to correct fixation. We also examined the time limit of final block (3000ms: no progress; 1000ms: maximal progress); % of trials with a correct fixation within the allowable window; and ‘Learning Rate’ calculated based on progression rates throughout training (see Supplement).
Author Manuscript
After final mood ratings, participants were asked in an open-ended format to state what was required to receive positive feedback during training. Responses were coded for presence/ absence of explicit rule knowledge. The Face in the crowd (FitC) task was used to assess generalization of training to a distinct visual search task (see Supplement) and for baseline pupillary assessment, as described below.
Emotion. Author manuscript; available in PMC 2017 February 01.
Price et al.
Page 4
Stress induction
Author Manuscript
The Critical Feedback Task (Rossi & Pourtois, 2012)(see Supplement) is a mental counting task with bogus negative feedback. Participants were told results reflect intelligence and asked to tally instances of rare lines with a different in-plane orientation from distractors. Differences in orientation are extremely difficult to notice, creating high uncertainty. Participants were told the difficulty of each block would depend on performance. Unknown to them, participants always started with the most difficult block (minimal difference between target and distractor angles). End-of-block feedback was always negative and the following block was always easier. Questionnaires
Author Manuscript
Two visual analogue scales (VAS) measured how happy and sad participants felt “at this moment” on a 0-10 scale (“not at all” to “very much”). The VAS scores used in primary analyses were collected just before and after the stress induction task (t3 & t4; Figure-1); additional VAS scores and secondary mood measures were not used in primary analyses, as the timing of assessments likely reduced sensitivity to stressor-related effects (see Supplement). Bonferonni correction was applied across the two primary measures; both corrected and uncorrected p-values are reported. Moderator analysis: Pupil dilation
Author Manuscript
Pupil diameter was recorded by the eyetracker throughout the pre-training FitC task and preprocessed (see Supplement). Analysis focused on the trial type containing 5 angry distractors and 1 happy target face (5Angry1Happy), which we expected to be most relevant to mood outcomes given high emotional content and the need for simultaneous disengagement from negative faces and engagement with positive faces. To assess moderation effects on mood, pre-post-stress change scores for each mood outcome (VAS Happy/Sad) were calculated. Hierarchical regression analyses, performed separately at every timepoint in the waveform, tested whether pupil × training-group interaction terms explained additional variance in VAS change, over and above main effects of group and pupil. Type I error was held at p
Emotion. Author manuscript; available in PMC 2017 February 01. Published in final edited form as: Emotion. 2016 February ; 16(1): 110–116. doi:10.1037/emo0000093.
A Novel Attention Training Paradigm Based on Operant Conditioning of Eye Gaze: Preliminary Findings Rebecca B. Price1, Inez M. Greven2, Greg J. Siegle1, Ernst H.W. Koster3, and Rudi De Raedt3 1University
Author Manuscript
2Bangor 3Ghent
of Pittsburgh School of Medicine, Pittsburgh, PA
University, Bangor, UK
University, Belgium
Abstract
Author Manuscript
Inability to engage with positive stimuli is a widespread problem associated with negative mood states across many conditions, from low self-esteem to anhedonic depression. Though attention retraining procedures have shown promise as interventions in some clinical populations, novel procedures may be necessary to reliably attenuate chronic negative mood in refractory clinical populations (e.g., clinical depression) through, e.g., more active, adaptive learning processes. In addition, a focus on individual difference variables predicting intervention outcome may improve the ability to provide such targeted interventions efficiently. To provide preliminary proof-ofprinciple, we tested a novel paradigm using operant conditioning to train eye gaze patterns towards happy faces. Thirty-two healthy undergraduates were randomized to receive operant conditioning of eye gaze towards happy faces (Train-Happy) or neutral faces (Train-Neutral). At the group level, the Train-Happy condition attenuated sad mood increases following a stressful task, in comparison to Train-Neutral. In individual differences analysis, greater physiological reactivity (pupil dilation) in response to happy faces (during an emotional face-search task at baseline) predicted decreased mood reactivity following stress. Preliminary results suggest that operant conditioning of eye gaze towards happy faces buffers against stress-induced effects on mood, particularly in individuals who show sufficient baseline neural engagement with happy faces. Eye gaze patterns to emotional face arrays may have a causal relationship with mood reactivity. Personalized medicine research in depression may benefit from novel cognitive training paradigms that shape eye gaze patterns through feedback. Baseline neural function (pupil dilation) may be a key mechanism, aiding in iterative refinement of this approach.
Author Manuscript
Keywords attentional bias; attention training; eyetracking; mood; pupil
Corresponding author information: Rebecca B. Price, University of Pittsburgh School of Medicine, Pittsburgh, [email protected].
Price et al.
Page 2
Author Manuscript
Introduction
Author Manuscript
Cognitive biases away from positive information, and towards negative information, are posited to play a critical role in the etiology and maintenance of negative affective conditions (e.g., Gotlib & Joormann, 2010) by promoting hyper-awareness of negative information, limiting awareness of positive information, and reinforcing maladaptive beliefs (e.g., Clark, Beck, & Alford, 1999; de Raedt & Koster, 2010). A growing literature suggests attention retraining techniques designed to modify attentional bias can effectively reduce clinical symptoms (MacLeod & Clarke, 2015). However, while these techniques appear to have relatively robust effects on some conditions (e.g., clinical anxiety), results of extant attention retraining studies in the context of other disorders (e.g., acute depression) have been mixed (reviewed by Mogoase, David, & Koster, 2014). Novel strategies to ameliorate attentional bias may help to address this gap in the clinical applicability of attention retraining techniques and broaden the range of individuals who might receive benefit.
Author Manuscript
Here, we sought to 1) provide preliminary proof-of-principal for one such novel strategy— operant (feedback-based) conditioning of eye gaze towards happy faces—by testing its effects on mood reactivity in a healthy sample, and 2) identify individual differences in neural engagement (indexed by pupil dilation) at baseline that can predict favorable response to the strategy, as an integral step towards further intervention refinement. Several specific features of the training paradigm were selected in the hopes of maximizing translational relevance to depressive patients. Foremost was an active, adaptive, operant learning process utilizing positive feedback—an effective means of enhancing learning (Masters, Maxwell, & Eves, 2009). We also used a training goal of increased focus on positive stimuli, designed to remediate a key attentional pattern in depression (e.g., Gotlib, McLachlan, & Katz, 1988); relatively ecologically valid stimuli (arrays of twelve emotional faces)(Dandeneau & Baldwin, 2004); and on-line, continuous measurement of eye gaze patterns to provide information proximal to the modification of visual gaze itself, rather than more ambiguous and complex measures such as manual response latencies.
Author Manuscript
Even if mood improvement is observed at the group level, individual differences in neural engagement may moderate training effects (Collier & Siegle, 2015; Siegle et al., 2014), providing clues for what psychophysiological processes must be engaged to maximize benefit. Thus, the second goal of the study was to evaluate baseline neural engagement as a predictor of post-training mood reactivity, using pupil dilation as a marker of neural engagement (Beatty, 1986; Koikegami & Yoshida, 1953) during a relevant face-search task. Consistent with previous pupil findings in depression (Collier & Siegle, 2015; Siegle et al., 2014), we specifically hypothesized that greater neural engagement with training-relevant stimuli (here, happy faces; i.e., greater pupil dilation when happy faces were presented) would predict more favorable post-training mood outcomes. Incorporating neurophysiological moderator analysis from the earliest stages of intervention development strongly promotes the ability to identify key intervention targets and make iterative refinements to expand the intervention’s reach, if and when dissemination becomes warranted.
Emotion. Author manuscript; available in PMC 2017 February 01.
Price et al.
Page 3
Author Manuscript
Method Participants Thirty-two healthy undergraduates (mean=20.56y, SD=3.94; 8 male), were randomized to experimental vs. control training (n=16/group) and completed the protocol (Figure-1). The local ethics committee approved the study. Informed consent was obtained from all participants. Operant conditioning of eye movements
Author Manuscript
We trained participants to direct their attention towards a specific emotion (experimental condition: happy; control condition: neutral). Following a fixation cross (presented until 250ms gaze fixation was detected), pictures of 12 different women from the NimStim set were presented pseudo-randomly in a diamond pattern. Six different emotional expressions were displayed (happy, angry, sad, fearful, disgusted, neutral—two faces per emotion; details in Supplement). Participants were instructed to attentively observe the pictures and were told they would hear a short, positive sound after responding “correctly.” No further instructions were given. When participants fixated on the target stimulus for 250ms within the time limit, a short sound designated correct completion. Otherwise, the trial ended and the experiment continued without feedback.
Author Manuscript
Participants were presented with at least 4 blocks of 36 trials. The first block began with a trial time limit of 3000ms. Continuation to faster blocks was adaptively based on performance. If 80% or more of trials were completed correctly, the time limit was decreased by 500ms (until the last block, which had a 1000ms limit). Otherwise, that speed was repeated. The experiment automatically stopped after the same speed was repeated 3 times (4 times for the initial block). Behavioral outcomes of training Training success was assessed using data from each participant’s first and last block. The primary outcome was latency to correct fixation. We also examined the time limit of final block (3000ms: no progress; 1000ms: maximal progress); % of trials with a correct fixation within the allowable window; and ‘Learning Rate’ calculated based on progression rates throughout training (see Supplement).
Author Manuscript
After final mood ratings, participants were asked in an open-ended format to state what was required to receive positive feedback during training. Responses were coded for presence/ absence of explicit rule knowledge. The Face in the crowd (FitC) task was used to assess generalization of training to a distinct visual search task (see Supplement) and for baseline pupillary assessment, as described below.
Emotion. Author manuscript; available in PMC 2017 February 01.
Price et al.
Page 4
Stress induction
Author Manuscript
The Critical Feedback Task (Rossi & Pourtois, 2012)(see Supplement) is a mental counting task with bogus negative feedback. Participants were told results reflect intelligence and asked to tally instances of rare lines with a different in-plane orientation from distractors. Differences in orientation are extremely difficult to notice, creating high uncertainty. Participants were told the difficulty of each block would depend on performance. Unknown to them, participants always started with the most difficult block (minimal difference between target and distractor angles). End-of-block feedback was always negative and the following block was always easier. Questionnaires
Author Manuscript
Two visual analogue scales (VAS) measured how happy and sad participants felt “at this moment” on a 0-10 scale (“not at all” to “very much”). The VAS scores used in primary analyses were collected just before and after the stress induction task (t3 & t4; Figure-1); additional VAS scores and secondary mood measures were not used in primary analyses, as the timing of assessments likely reduced sensitivity to stressor-related effects (see Supplement). Bonferonni correction was applied across the two primary measures; both corrected and uncorrected p-values are reported. Moderator analysis: Pupil dilation
Author Manuscript
Pupil diameter was recorded by the eyetracker throughout the pre-training FitC task and preprocessed (see Supplement). Analysis focused on the trial type containing 5 angry distractors and 1 happy target face (5Angry1Happy), which we expected to be most relevant to mood outcomes given high emotional content and the need for simultaneous disengagement from negative faces and engagement with positive faces. To assess moderation effects on mood, pre-post-stress change scores for each mood outcome (VAS Happy/Sad) were calculated. Hierarchical regression analyses, performed separately at every timepoint in the waveform, tested whether pupil × training-group interaction terms explained additional variance in VAS change, over and above main effects of group and pupil. Type I error was held at p
