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Cognitive reappraisal in an unpredictable world: Prior context matters
International Journal of Psychophysiology 146 (2019) 173–179
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International Journal of Psychophysiology journal homepage: www.elsevier.com/locate/ijpsycho
Cognitive reappraisal in an unpredictable world: Prior context matters Michael J. Imburgio , Annmarie MacNamara ⁎
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Department of Psychological and Brain Sciences, Texas A&M University, College Station, TX, USA
ARTICLE INFO
ABSTRACT
Keywords: Emotion regulation Late positive potential Event-related potential ERP LPP Unpredictability
Cognitive reappraisal is a higher order emotion regulation strategy, the effects of which can be measured using the late positive potential (LPP), an event-related potential that is larger for emotional versus neutral stimuli. Whereas the lab provides a relatively predictable and calm environment in which to engage in reappraisal, outside of the lab, individuals may need to enact reappraisal in unpredictable and anxiety-provoking environments. In prior work, unpredictable auditory tones have been shown to increase threat-processing and induce anxiety. Here, forty-seven participants performed a reappraisal task while being exposed in a blockwise fashion to a “Random Tone” sequence or silence (“No Tone”), to determine the effects of an unpredictable auditory stimulus on the reappraisal of negative pictures. In addition, exploratory analyses assessed whether starting block (i.e., beginning the task in a Random Tone versus No Tone block) would moderate effects. Results showed that during an early time window, reappraisal LPPs were smallest for participants who started in a No Tone block and who performed reappraisal in a No Tone block. Therefore, reappraisal may be optimally performed when conditions are predictable/calm, by participants whose initial learning context was also predictable/calm. In addition, larger LPPs for negative versus neutral images were only observed throughout the later portion of picture presentation for participants who began in a Random Tone block, suggesting that unpredictability may increase sustained attention towards aversive stimuli. The results fit within a growing body of work aimed at understanding contextual and individual differences in emotion regulation.
1. Introduction When implemented effectively, emotion regulation has mental, physical and social benefits (Denny and Ochsner, 2014; Haga et al., 2009; Quoidbach et al., 2010). On the other hand, difficulties implementing emotion regulation are associated with reduced psychological wellbeing and may play a role in the development and maintenance of disorders such as anxiety and depression (Campbell-Sills and Barlow, 2007). Over the past several years, cognitive reappraisal, an emotion regulation strategy that involves changing the meaning of a stimulus, has been studied extensively in the lab. For example, evidence suggests that when instructed to do so, both healthy and clinical samples can effectively down-regulate their response to emotional stimuli using reappraisal (McRae et al., 2008, 2012; Ray et al., 2010; Smoskia et al., 2013; but see Morris et al., 2012). In laboratory settings, reappraisal may be relatively straightforward. However, in the real world, reappraisal may be most needed in unpredictable, stress-inducing and distracting environments. Here, we sought to examine how an unpredictable context might compromise reappraisal, and whether individual differences in prior exposure to an unpredictable or calm context might modulate these effects. ⁎
Prior work has examined how stressful mood manipulations may affect subsequent attempts to reappraise. For example, Raio et al. (2013) asked participants to complete a threat-learning procedure in which they learned to associate one picture (a conditioned stimulus, CS +) with an aversive outcome but not another (CS−). Next, participants were trained in reappraisal and were explicitly instructed to reappraise the CS+. Twenty-four hours later, participants returned to the lab and were exposed to a physiological stressor (i.e., cold pressor test) or to a control condition, before completing the threat conditioning task again while employing their newly learned reappraisal skills. Results showed that the non-stressed group had reduced skin conductance responses to the CS+ following training in reappraisal, whereas the stressed group showed no such benefits (Raio et al., 2013). Therefore, an acute stressor may negatively affect participants' subsequent ability to implement reappraisal. On the other hand, however, some work has suggested that reappraisal is relatively resistant to stress. For example, Shermohammed et al. (2017) found that participants who underwent a psychosocial stressor (Trier Social Stress Test; Kirschbaum et al., 1993) showed no decrement in reappraisal ability, compared to participants in a control group. As such, evidence regarding the effect of stress on reappraisal has been mixed and results may depend on the type of stressor
Corresponding author at: Department of Psychological and Brain Sciences, Texas A&M University, 4235 TAMU, College Station, TX 77843, USA. E-mail address: [email protected] (M.J. Imburgio).
https://doi.org/10.1016/j.ijpsycho.2019.09.003 Received 27 February 2019; Received in revised form 30 August 2019; Accepted 9 September 2019 Available online 24 October 2019 0167-8760/ Published by Elsevier B.V.
International Journal of Psychophysiology 146 (2019) 173–179
M.J. Imburgio and A. MacNamara
employed. Whereas a stressful event might have a downstream effect on participants' subsequent ability to engage in cognitive reappraisal, contextual manipulations that take place simultaneous with reappraisal might be more powerful. In prior work, irregular auditory tones have been used to induce an unpredictable context that participants find anxiety-provoking (Jackson et al., 2015; Nelson et al., 2016). In addition, listening to an unpredictable tone sequence while performing another task increases the electrocortical processing of errors (Jackson et al., 2015; Speed et al., 2017) and reduces electrocortical responses to reward (Nelson et al., 2016). Unpredictable tones have been found to increase attention towards threat and amygdala activation in humans, and to increase anxiety-like behaviors and amygdala activation in mice (Herry et al., 2007). However, it is currently unknown whether unpredictable tones might also impair cognitive regulation of negative and neutral stimuli. It is also possible that the extent to which an unpredictable context might interfere with participants' ability to reappraise stimuli might depend on an individual's prior experiences with that context. For example, participants in a study by Diener et al. (2009) completed a paradigm in which they were told that they could press a button to avoid electric shock. However, while this was true for some blocks of the experiment (controllable stress), there were other blocks in which participants were unable to escape electric shock, despite their best efforts (i.e., regardless of their button presses; uncontrollable stress). Results showed that prior experiences of controllability appeared to buffer or “immunize” participants against future experiences of uncontrollability (as measured by ERP component, post-imperative negative variation, PINV), whereas initial experiences of uncontrollability seemed to render individuals more vulnerable to future encounters with these situations. Both controllability and predictability can attenuate stress responding (Abbott et al., 1984; Geer et al., 1970; Oka et al., 2010; Visintainer et al., 1982) and controllability may in part exert its effects on stress by increasing the predictability of unpleasant events (Geer and Maisel, 1972); therefore, we reasoned that the initial conditions under which an individual first learns to perform a reappraisal task (i.e., no tone versus unpredictable tones) might affect his/her subsequent ability to reappraise stimuli under distracting or unpredictable conditions. Here, we examined the effect of context on reappraisal by asking participants to reappraise negative pictures while simultaneously listening to unpredictable tones or no tone (Jackson et al., 2015; Nelson et al., 2016). In addition to this within-subjects manipulation, we assigned participants to begin the task in an unpredictable or no tone block. We used an event-related potential, the late positive potential (LPP), to assess the effects of reappraisal on the processing of negative and neutral pictures. The LPP is a centroparietally maximal ERP component that begins around 300 ms following stimulus onset and is larger for emotional compared to neutral stimuli (Cuthbert et al., 2000). The LPP is smaller when participants are asked to reappraise the meaning of negative pictures (Blechert et al., 2012; Fitzgerald et al., 2016; Hajcak and Nieuwenhuis, 2006; Moran et al., 2013; Thiruchselvam et al., 2011, but see Babkirk et al., 2015; Decicco et al., 2014; Dennis and Hajcak, 2009; Walker et al., 2011), indicating reduced picture processing. Participants in the current study performed a well-validated reappraisal task commonly used with the LPP (Hajcak and Nieuwenhuis, 2006), in which they were asked to reappraise or watch negative pictures, as well as to passively view neutral pictures. We hypothesized that negative pictures would elicit larger LPPs than neutral pictures, and that reappraisal would reduce the LPP to negative pictures. Additionally, we hypothesized that reappraisal would be less effective at modulating the LPP during unpredictable tone blocks compared to blocks on which no tone was presented. We also examined an exploratory hypothesis that participants who began with a no tone block might be less affected by the tones, as evidenced by reappraisal's effect on the LPP (Diener et al., 2009).
2. Method 2.1. Participants Sample size was determined by our a priori decision to run the study for a single semester, with the total N resulting from the number of undergraduates who signed up to complete the study during this time. The sample consisted of 54 undergraduates who completed the study for course credit. Seven participants were eliminated from analyses due to excessive artifacts during EEG recordings (i.e., on > 50% of trials), leaving a final sample of 47 participants (57% female, 41% male, 2% other; MAGE = 19.04 years; SD = 3.31). Study procedures were in compliance with the Helsinki Declaration of 1975 (as revised in 1983) and were approved by the Texas A&M University institutional review board. 2.2. Stimuli One hundred negative and 50 neutral pictures were selected from the International Affective Picture System (IAPS; Lang et al., 2008) and the Emotional Picture Set (EmoPicS; Wessa et al., 2010). The auditory tone sequence presented in some blocks was identical to that used in previous work (Herry et al., 2007; Jackson et al., 2015; Nelson et al., 2016). The random tones were generated by starting with a regular tone sequence (for which the carrier frequency was 100 Hz, pulse duration was 40 ms, and mean pulse spacing was 200 ms), then applying a random temporal shift to each tone in the regular sequence. The resulting random tones were presented to participants through headphones at 90 dB. 2.3. Reappraisal task The reappraisal task was modeled after those previously used (Hajcak and Nieuwenhuis, 2006; Moser et al., 2006); however, during some blocks, a random tone (described above) was played over headphones, while in other blocks no tone was played. At the beginning of the experiment, participants were trained in the reappraisal task. They were told that they would be viewing negative and neutral pictures and that negative pictures would be preceded by the word “WATCH” or “DECREASE” and neutral pictures would be preceded by the word “VIEW”. Participants were told that when they saw the word “WATCH” or “VIEW”, that they should simply view the picture as they normally would, without trying to change their response in any way. However, participants were instructed that when they saw the word “DECREASE” before presentation of a negative picture, they should try to reduce their emotional response to the picture by changing its meaning. For example, if viewing a picture of a house fire, participants could tell themselves that help was on the way and everyone would survive, or for a photo of a gruesome war scene, they could tell themselves that the picture was taken from a movie and no one was really hurt. Participants viewed negative pictures and the experimenter provided examples of how participants could reappraise those pictures. Following this, participants completed five practice trials to become familiar with the paradigm. After each practice picture that had been preceded by the word “DECREASE”, the experimenter asked the participant how they had attempted to reduce their emotional response and provided guidance or feedback as necessary (i.e., to ensure participants understood directions and were using cognitive reappraisal; Parvaz et al., 2012). Once they had been trained in and had practiced the reappraisal task, participants were told that they would also hear some tones played over headphones during some portions of the experiment and that these tones were unrelated to their task. Following these instructions, participants completed the task while continuous electroencephalography (EEG) was recorded. The task was broken into six blocks – three blocks in which participants listened to a random sequence of tones throughout the entire block (“Random 174
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condition (No Tone, Random Tone) on the LPP were examined using mixed linear models in which picture condition, tone condition and starting block were fixed factors and participant was a random factor. Analyses were performed separately for each LPP time window. Linear models were fit using the lme4 package (Bates et al., 2008) with p values estimated using the lmerTest package (Kuznetsova et al., 2017). When necessary, significant interactions were followed up by comparisons of estimated marginal means with Bonferroni-corrected p-values using the emmeans package (Lenth and Herve, 2018). We chose to examine these effects using mixed linear models rather than mixed between-within ANOVAs because they allowed us to formally test whether the inclusion of the starting block factor and associated interaction terms accounted for a significant proportion of variance. We began with a model including the fixed factors, picture condition and tone condition, their interaction term, and random factor, participant. We then tested whether introducing the fixed factor, starting block and all associated interaction terms to the model accounted for a significant proportion of additional variance using a maximum likelihood ratio test. To account for the exploratory nature of these tests and given that we had already performed one set of tests, we used a more stringent significance threshold of p = .05/2 = .025. Theoretically, mixed linear models can also better account for unequal group sizes (i.e., in each level of the starting block factor; Bagiella et al., 2000). In addition, the lmerTest and emmeans packages use the Satterthwaite method of estimating degrees of freedom, which does not assume equal variances across groups, better models heterogeneity among groups and subjects, and better controls for Type I error in the case of mixed models when compared to a traditional residual df approximation (Keselman et al., 1999). Nonetheless, it should be noted that using mixed between-within ANOVAs that were GreenhouseGeisser corrected for violations of sphericity yielded conclusions in line with those presented here.
Tone”) and three blocks in which no tones were played (“No Tone”). Trials were also blocked by picture type; this resulted in one neutral, two negative Random Tone blocks and one neutral, two negative No Tone blocks, each containing 25 trials. Participants were informed about the picture type at the beginning of each block (e.g., “In this block you will see only negative pictures”). An even number of “WATCH”, “REAPPRAISE” and “VIEW” trials were presented in Random Tone and No Tone blocks and trials were presented in random order. Therefore, there were 150 trials in total: 25 No Tone “VIEW” neutral trials; 25 random tone “VIEW” neutral trials; 25 no tone “WATCH” negative trials; 25 random tone “WATCH” negative trials; 25 no tone “REAPPRAISE” negative trials and 25 random tone “REAPPRAISE” negative trials. Each trial began with a 2000 ms presentation of the word, “VIEW” (for neutral trials), “WATCH” (for passive viewing negative trials), or “DECREASE” (for reappraise negative trials). Next, participants viewed a white fixation cross on a black background for 500 ms; this was followed by a negative or neutral picture that was presented for 6000 ms. Each trial was separated by a white fixation cross presented on a black background for 2000–2500 ms. Pictures were randomly selected from the neutral and negative picture sets and each picture was shown exactly once during the task. Participants were randomized to begin with either a No Tone (N = 21) or Random Tone (N = 26) block and block order was randomized across the remainder of trials for each participant. 2.4. EEG recording and processing Continuous EEG was recorded using an ActiCap and the ActiChamp amplifier (Brain Products, Gilching Germany). Thirty-two electrode sites were used based on the 10/20 system. The electrooculogram (EOG) was recorded from four facial electrodes: two electrodes were placed approximately 1 cm above and below the right eye, forming a bipolar channel to measure vertical eye movement and blinks and two electrodes were placed approximately 1 cm beyond the outer edge of each eye, forming a bipolar channel to measure horizontal eye movements. EEG data was digitized at a 24-bit resolution with a sampling rate of 500 Hz. EEG data were processed offline using BrainVision Analyzer 2 software (Brain Products GmbH, Gilching, Germany). Data were segmented for each trial beginning 200 ms before picture onset and lasting for 6200 ms (i.e., for the entire picture duration). The signal from each electrode was referenced offline to the average of the left and right mastoids (TP9/10) and band-pass filtered with high-pass and low-pass filters of 0.01 and 30 Hz, respectively. Eye blink and ocular corrections used the method developed by Miller et al. (1988). Artifact analysis was used to identify a voltage step of > 50.0 μV between sample points, a voltage difference of 300.0 μV within a trial, and a maximum voltage difference of < 0.50 μV within 100-ms intervals. Trials were also inspected visually for any remaining artifacts, and data from individual channels containing artifacts were rejected on a trial-to-trial basis. The number of retained trials did not differ by condition, F(5,276) = 0.18, p = .97 (Random Tone, Neutral View M = 23.68, SD = 1.85; Random Tone, Negative Watch M = 23.68, SD = 1.78; Random Tone, Negative Reappraise M = 23.68, SD = 2.00; No Tone, Neutral View M = 23.92, SD = 1.40; No Tone, Negative Watch M = 23.50, SD = 1.95; No Tone, Negative Reappraise M = 23.70, SD = 2.07; Min = 14, Max = 25). The LPP was scored by averaging amplitudes from three frontocentral sites at which it was maximal (FC1, FC2, and Cz), during an early time window (400–3200 ms) and a late time window (3200–6000 ms).
3. Results Grand-average waveforms for each combination of picture and tone condition are presented in Fig. 1. Headmaps corresponding to the voltage difference for Negative Watch minus Neutral View and Negative Reappraise minus Neutral View are also shown in Fig. 1. Fig. 2 depicts grand-average waveforms for each condition, shown separately for Random Tone blocks and No Tone blocks. Table 1 presents mean amplitudes at the frontocentral pooling for the early and late time windows, shown separately for each picture and tone condition as well as each starting block. 3.1. LPP (400–3200 ms) The inclusion of the starting block factor accounted for a significant proportion of variance beyond that accounted for by the model including only picture condition and tone condition, χ2(6) = 25.11, p < .001; therefore, only results from the full model are reported below. Significant main effects of picture condition, F(2,225) = 31.45, p < .001 (Negative Watch > Neutral View, t[225] = 6.65, p < .001, β = 0.58; Negative Reappraise > Neutral View, t[225] = 7.07, p < .001, β = 0.62; Negative Watch vs. Negative Reappraise, t [225] = 0.43, p = 1.00), starting block X picture condition, F (2,225) = 4.16, p = .02 (Random Tone first, Negative Reappraise > No Tone First, Negative Reappraise, t[45] = 2.37, p = .02, β = 0.60; Random Tone first, Negative Watch vs. No Tone first, Negative Watch, p = .07; Random Tone first, Neutral View vs. No Tone first, Neutral View, p = .47) and starting block X tone condition, F(2,225) = 5.14, p = .02 (Random Tone first, No Tone Block > No Tone First, No Tone Block, t[45] = 2.51, p = .02, β = 0.56; Random Tone first, Random Tone Block vs. No Tone first, Random Tone Block, p = .26) were qualified by a three-way interaction between starting block X picture condition X tone condition, F(2,225) = 4.11, p = .02. Follow-up tests
2.5. Data analyses Data analyses were conducted using R version 3.5.1 (R Core Team, 2016). The effects of picture condition (Netural View, Negative Watch, Negative Reappraise), starting block (No Tone, Random Tone) and tone 175
International Journal of Psychophysiology 146 (2019) 173–179
M.J. Imburgio and A. MacNamara
Fig. 1. Grand-average waveforms depict amplitudes at the frontocentral pooling where the LPP was scored, shown separately for each condition; the vertical dashed line denotes the end of the early time window and the beginning of the late time window. Headmaps show the spatial distribution of voltage differences for Negative Watch minus Neutral View trials (top) and Negative Reappraise minus Neutral View trials (bottom), shown separately for each time window in which the LPP was scored. Shaded areas depict pooled SEM of the groups across both windows.
Fig. 2. Grand-average waveforms depict amplitudes at the frontocentral pooling where the LPP was scored, shown separately for each picture condition and group in No Tone blocks (top) and Random Tone blocks (bottom); the vertical dashed line denotes the end of the early time window and the beginning of the late time window. Shaded areas depict pooled SEM of the groups across both windows.
performed separately within each picture condition1 revealed a significant starting block X tone condition interaction within Negative Reappraise, F(1,45) = 16.65, p < .001, but not within Negative Watch (p = .94) or Neutral View (p = .83). Follow-up tests revealed that No Tone first, No Tone Reappraise was smaller than the other three Reappraisal cells (Table 1). The results of these tests were as follows: Random Tone first, No Tone Reappraise > No Tone first, No Tone Reappraise, t(43.16) = 3.58, p < .001, β = 0.94; Random Tone first,
Random Tone reappraise > No Tone first, No Tone Reappraise, t (37.77) = 3.29, p = .002, β = 0.89; No Tone first, Random Tone reappraise > No Tone first, No Tone Reappraise, t(20) = 5.31, p < .001, β = 0.68. There were no differences between the other three cells (all ps > .26). No other effects reached significance in the full model, ps > .06. 3.2. LPP (3200–6000 ms) The inclusion of the starting block factor accounted for a significant proportion of variance beyond that accounted for by the model including only picture condition and tone condition, χ2(6) = 16.21, p = .01; therefore, only results from the full model are reported below. A main effect of picture condition, F(2,225) = 11.45, p < .001, was qualified by a two-way interaction between starting block X picture condition, F(2,225) = 4.05, p = .02, which showed that negative pictures elicited larger LPPs than neutral pictures for participants that had started with a Random Tone block (main effect of picture condition, F
1
Another way to interpret this interaction would have been to compare picture conditions separately within each tone condition. For example, this might have revealed that reappraisal reduced the LPP in one tone condition but not the other. For participants that completed a No Tone block first, the difference between Negative Reappraise and Negative Watch trials did not reach significance within No Tone blocks (p = .35, β = 0.34) or within Random Tone blocks (p = .12, β = 0.33). Nonetheless, condition means were in opposite directions: Negative Watch > Negative Reappraise in the No Tone blocks and Negative Reappraise > Negative Watch in the Random Tone blocks. 176
International Journal of Psychophysiology 146 (2019) 173–179
M.J. Imburgio and A. MacNamara
Table 1 Means (standard deviations) for the LPP, shown separately for each time window, condition and group. Early window (400–3200 ms)
Neutral view Negative watch Negative reappraise
Late window (3200–6000 ms)
Random tone block first
No tone block first
Random tone (μv)
No tone (μv)
Random tone (μv)
1.89 (3.94) 6.42 (5.49) 6.29 (4.54)
2.07 (3.60) 6.43 (6.77) 7.28 (5.78)
1.16 (6.40) 3.30 (6.32) 5.37 (5.75)
Random tone block first
No tone block first
No tone (μv)
Random tone (μv)
No tone (μv)
Random tone (μv)
No tone (μv)
1.07 (4.57) 3.20 (6.67) 1.25 (5.71)
1.82 (3.94) 7.55 (5.17) 4.64 (4.66)
2.75 (4.21) 6.97 (5.59) 6.41 (6.56)
2.31 (8.50) 2.90 (8.57) 4.79 (8.53)
1.89 (5.66) 3.64 (10.86) 2.20 (9.36)
served as contextual conditioning for learning that took place throughout this first block. That is, although we trained participants on cognitive reappraisal before they began the task, participants' skill and comfort level with the task likely continued to increase throughout the first block. If learning took place during the first block in the absence of unpredictable tones, this might explain why participants were more likely to experience interference during subsequently presented unpredictable blocks. Taken as context-dependent learning, the effects of the current study are in line with prior work that asked participants to encode and recall information either in a stressful context (while skydiving) or a calm context (on the ground; Thompson et al., 2001). Results showed that, for participants who learned information under calm conditions, a stressful context decreased performance compared to a calm context. On the other hand, for participants who learned information while skydiving, recall was poor independent of retrieval context. Therefore, as in the current study, participants who learned in a calm context were selectively sensitive to the subsequent introduction of a stressful context, whereas a stressful context during learning hindered performance more broadly. As such, the current results support the notion that affect plays a role in cognitive control. Moreover, our results suggest a role for historical affective context. That is, either a current or historical unpredictable context appears to compromise reappraisal, as compared to reappraisal as it is typically performed in the lab (i.e., free from auditory tones). Nonetheless, we caution that other, non-affective mechanisms might also explain the current results. That is, in addition to inducing stress or anxiety, the unpredictable tones might have been distracting – perhaps especially for participants who first acclimated to the task in the absence of the tones. In keeping with this, prior work found that individuals who had been exposed to a less distracting context were more susceptible to the effects of distraction during subsequent task performance than individuals who had previously been exposed to a noisy or distracting context. Additionally, participants who were accustomed to distracting contexts experienced generalized performance deficits independent of future distractions (Heft, 1979). Furthermore, biased competition models of attention suggest that distraction most often interferes with cognitive tasks that rely heavily on the frontal lobe (Lavie, 2005), such as cognitive reappraisal (see Buhle et al., 2014), which could explain why we observed interference for the reappraisal condition in particular. During the later portion of picture presentation, negative pictures ceased to elicit an increased LPP for participants who had begun the task with a toneless block. On the other hand, participants who were first exposed to the unpredictable tone sequence continued to show larger LPPs for negative compared to neutral images throughout the later portion of picture presentation. Prior work suggests that unpredictable tone sequences may increase participants' attention towards aversive stimuli. For example, while listening to unpredictable tones, participants were more likely to orient towards angry faces rather than neutral faces (Herry et al., 2007) and to show increased electrocortical processing of errors, which can be viewed as internal threats (Jackson et al., 2015). Therefore, individuals who began the task in the unpredictable tone condition may have learned to engage more with the
[2,128] = 18.03, p < .001, Negative Reappraise versus Neutral View, t [128] = 3.86, p < .001, β = 0.59; Negative Watch versus Neutral View, t[128] = 5.91, p < .001, β = 0.92; Negative Watch versus Negative Reappraise, p = .10), but not for participants who had started with a No Tone block (main effect of picture condition, p = .38). No other effects reached significance in the full model, ps > .10. 4. Discussion Cognitive reappraisal is a complex, higher-order emotion regulation strategy that relies on an orchestrated set of mental operations and may be vulnerable to interference from contextual factors. Work examining the effect of stress manipulations on cognitive reappraisal has yielded mixed results (Raio et al., 2013; Shermohammed et al., 2017). However, no work to date has examined how unpredictability might modulate reappraisal's effects on neural activity, or how an individual's history with an unpredictable context might affect reappraisal. Here, we examined the effect of a random auditory tone (versus no tone) on the reappraisal of negative images, as measured by the LPP. Results showed that early reappraisal LPPs were smallest for participants who started in a No Tone block and who performed reappraisal in a No Tone block. Therefore, reappraisal may be optimally performed when conditions are predictable/calm, by participants whose initial learning context was also predictable/calm. In addition, whereas negative pictures elicited larger LPPs than neutral pictures across all participants in the early time window, only participants who began the experiment in a Random Tone block showed larger LPPs to negative compared to neutral pictures, in the late time window. This pattern of results suggests that initial exposure to an unpredictable context might increase the sustained processing of negative stimuli. Given that both predictability and controllability can attenuate physiological stress responding (Abbott et al., 1984; Geer et al., 1970; Oka et al., 2010; Visintainer et al., 1982), we had expected that beginning the task in the no tone condition might protect participants from their deleterious effects on reappraisal. This hypothesis was based on the work of Diener et al. (2009), who found that participants who began a task with control over shock exposure showed more normative electrocortical responding than participants who began the study with no control over the shock (Diener et al., 2009). Here, results differed, in that participants who had started in a No Tone block were most affected by the unpredictable tones, showing larger early reappraisal LPPs (compared to the No Tone condition). Task differences may in part explain divergence between the current results and prior findings. First, despite their similarities, uncontrollability and unpredictability are distinct phenomena and may elicit dissociable effects (Baker and Stephenson, 2000). Second, in the current study, unpredictable tones were unrelated to participants' task, which was to reappraise pictures. By contrast, in Diener et al. (2009), controllability was central to and in line with the task instructions, in which participants were told that they could press a button to avoid shock delivery. Therefore, an initial experience of controllability in the Diener study may have reinforced participants' sense of self-efficacy and belief in the task instructions. Here, the tone condition during participants' starting block may have 177
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aversive or threatening aspects of pictures, leading to prolonged processing of negative pictures throughout the study. Reappraisal of negative images did not significantly reduce the LPP, irrespective of starting block or tone condition. Though not in line with our prediction, these results are in accordance with several other studies that have also failed to observe a reduction in the LPP following reappraisal (Babkirk et al., 2015; Decicco et al., 2014; Dennis and Hajcak, 2009; Walker et al., 2011). One possibility is that reappraisal is more difficult for some pictures than others, such as those that are highly arousing (Langeslag and Surti, 2017); as such, reappraisal may have been more effective on some trials than others, reducing the effect size across the experiment. Additionally, reappraisal is a cognitively demanding technique: individuals must rapidly generate an alternative explanation for a stimulus and then must sustain and elaborate on this explanation throughout the duration of stimulus presentation. Therefore, individual variability in the implementation of this technique is to be expected; moreover, changing contexts and unpredictable tones may have made our task particularly challenging. Nonetheless, we note that although reappraisal did not significantly reduce the LPP across participants, individuals who began the task in the No Tone condition showed descriptively smaller LPPs during reappraisal compared to passive viewing of negative pictures. The next generation of emotion regulation research is likely to include a focus on understanding individual differences in emotion regulation, particularly as they pertain to emotion regulation that takes place outside of the lab. Ironically, reappraisal may be most needed in unpredictable or stressful situations, yet it may typically be first introduced in a predictable and safe environment, such as a therapist's office (e.g., in cognitive therapy). In order to help reappraisal skills generalize, future work may wish to examine how best to prepare individuals to reappraise in unpredictable environments. Additionally, a better understanding of the mechanisms underlying contextual effects on reappraisal is needed, including accounting for the potential contributions of anxiety, stress, and distraction. While the random tones employed in the current work have previously been found to invoke anxiety and orienting towards aversive stimuli (Jackson et al., 2015; Nelson et al., 2016), a limitation of the current study is that we did not have subjective ratings to determine whether the tones led to increased anxiety during reappraisal. Similarly, the current work relied solely on the LPP to assess reappraisal's effects on picture processing. Therefore, future work might wish to include subjective picture ratings and to assess associations between these ratings and the LPP. Finally, we used a no tone control condition because we thought that even predictable tones might interfere with a demanding cognitive task like reappraisal. If, however, similar effects were observed using predictable tones as a control condition, this might help rule out distraction or other non-specific effects as a potential explanation. Although the no tone control condition was likely more predictable than the random tones condition, it might not constitute a purely predictable context. Future work might wish to examine the effects of introducing a predictable context on reappraisal ability. In sum, previous work has examined cognitive reappraisal independent of context, even though context likely has a great effect on an individual's ability to regulate their emotions (Aldao, 2013). The results presented here suggest that an individual's prior experience may moderate the effect of context on emotion regulation. As such, the current work provides a means of understanding individual variation in reappraisal ability, and serves as groundwork for future work aimed at tailoring emotion regulation training and strategy to the individual.
References Abbott, B.B., Schoen, L.S., Badia, P., 1984. Predictable and unpredictable shock: behavioral measures of aversion and physiological measures of stress. Psychol. Bull. 96, 45–71. https://doi.org/10.1037/0033-2909.96.1.45. Aldao, A., 2013. The future of emotion regulation research: capturing context. Perspect. Psychol. Sci. 8, 155–172. https://doi.org/10.1177/1745691612459518. Babkirk, S., Rios, V., Dennis, T.A., 2015. The late positive potential predicts emotion regulation strategy use in school-aged children concurrently and two years later. Dev. Sci. 18, 832–841. https://doi.org/10.1111/desc.12258. Bagiella, E., Sloan, R.P., Heitjan, D.F., 2000. Mixed-effects models in psychophysiology mixed-effects models in psychophysiology. Psychophysiology 14, 13–20. Baker, S.R., Stephenson, D., 2000. Prediction and control as determinants of behavioural uncertainty: effects on task performance and heart rate reactivity. Integrative Physiological and Behavioral Science. https://doi.org/10.1007/BF02688786. Bates, D., Maechler, M., Dai, B., 2008. The lme4 Package, version 0.999375-26. http:// cran.r-project.org. Blechert, J., Sheppes, G., Tella, C., Williams, H., Gross, J.J., 2012. See what you think: reappraisal modulates behavioral and neural responses to social stimuli. Psychol. Sci. 23, 346–353. https://doi.org/10.1177/0956797612438559. Buhle, J.T., Silvers, J.A., Wage, T.D., Lopez, R., Onyemekwu, C., Kober, H., Webe, J., Ochsner, K.N., 2014. Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb. Cortex 24, 2981–2990. https://doi.org/10.1093/ cercor/bht154. Campbell-Sills, L., Barlow, D.H., 2007. Incorporating emotion regulation into conceptualizations and treatments of anxiety and mood disorders, Handbook of Emotion Regulation. The Guilford Press, New York, NY. Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., Lang, P.J., 2000. Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol. Psychol. 52, 95–111. https://doi.org/10.1016/S0301-0511(99) 00044-7. Decicco, J.M., Otoole, L.J., Dennis, T.A., 2014. The late positive potential as a neural signature for cognitive reappraisal in children. Dev. Neuropsychol. 39, 497–515. https://doi.org/10.1080/87565641.2014.959171. Dennis, T.A., Hajcak, G., 2009. The late positive potential: a neurophysiological marker for emotion regulation in children. J. Child Psychol. Psychiatry Allied Discip. 50, 1373–1383. https://doi.org/10.1111/j.1469-7610.2009.02168.x. Denny, B.T., Ochsner, K.N., 2014. Behavioral effects of longitudinal training in cognitive reappraisal. Emotion 14, 425–433. https://doi.org/10.1037/a0035276. Diener, C., Struve, M., Balz, N., Kuehner, C., Flor, H., 2009. Exposure to uncontrollable stress and the postimperative negative variation (PINV): prior control matters. Biol. Psychol. 80, 189–195. https://doi.org/10.1016/j.biopsycho.2008.09.002. Fitzgerald, J.M., MacNamara, A., DiGangi, J.A., Kennedy, A.E., Rabinak, C.A., Patwell, R., Greenstein, J.E., Proescher, E., Rauch, S.A.M., Hajcak, G., Phan, K.L., 2016. An electrocortical investigation of voluntary emotion regulation in combat-related posttraumatic stress disorder. Psychiatry Res. - Neuroimaging 249, 113–121. https:// doi.org/10.1016/j.pscychresns.2015.12.001. Geer, J.H., Maisel, E., 1972. Evaluating the effects of the prediction-control confound. J. Pers. Soc. Psychol. 23, 314–319. https://doi.org/10.1037/h0033122. Geer, J.H., Davison, G.C., Gatchel, R.I., 1970. Reduction of stress in humans through nonveridical perceived control of aversive stimulation. J. Pers. Soc. Psychol. 16, 731–738. https://doi.org/10.1037/h0030014. Haga, S.M., Kraft, P., Corby, E.K., 2009. Emotion regulation: antecedents and well-being outcomes of cognitive reappraisal and expressive suppression in cross-cultural samples. J. Happiness Stud. 10, 271–291. https://doi.org/10.1007/s10902-007-9080-3. Hajcak, G., Nieuwenhuis, S., 2006. Reappraisal modulates the electrocortical response to unpleasant pictures. Cogn. Affect. Behav. Neurosci. 6, 291–297. https://doi.org/10. 3758/CABN.6.4.291. Heft, H., 1979. Background and focal environmental conditions of the home and attention in young children. J. Appl. Soc. Psychol. 9, 47–69. https://doi.org/10.1111/j.15591816.1979.tb00794.x. Herry, C., Bach, D.R., Esposito, F., Di Salle, F., Perrig, W.J., Scheffler, K., Luthi, A., Seifritz, E., 2007. Processing of temporal unpredictability in human and animal amygdala. J. Neurosci. 27, 5958–5966. https://doi.org/10.1523/JNEUROSCI.521806.2007. Jackson, F., Nelson, B.D., Proudfit, G.H., 2015. In an uncertain world, errors are more aversive: evidence from the error-related negativity. Emotion 15, 12–16. https://doi. org/10.1037/emo0000020. Keselman, H.J., Kowalchuk, R.K., Algina, J., Wolfinger, R.D., 1999. The analysis of repeated measurements: a comparison of mixed-model Satterthwaite F tests and a nonpooled adjusted degrees of freedom multivariate test. Commun. Stat. - Theory Methods. https://doi.org/10.1080/03610929908832460. Kirschbaum, C., Pirke, K.M., Hellhammer, D.H., 1993. The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76–81. https://doi.org/10.1159/000119004. Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., 2017. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82. https://doi.org/10.18637/jss.v082. i13. Lang, P.J., Bradley, M.M., Cuthbert, B.N., 2008. International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual (Rep. No. A-8). (Gainsville, FL). Langeslag, S.J.E., Surti, K., 2017. The effect of arousal on regulation of negative emotions using cognitive reappraisal: an ERP study. Int. J. Psychophysiol. 118, 18–26. https:// doi.org/10.1016/j.ijpsycho.2017.05.012. Lavie, N., 2005. Distracted and confused?: selective attention under load. Trends Cogn.
Acknowledgements Thanks to Blake Barley for his assistance in data collection and processing. Thanks to Greg Hajcak for providing the unpredictable tone sequence. Annmarie MacNamara is supported by National Institute of Mental Health grant, K23MH105553. 178
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M.J. Imburgio and A. MacNamara Sci. https://doi.org/10.1016/j.tics.2004.12.004. Lenth, R.L., Herve, M., 2018. Emmeans: Estimated Marginal Means, aka Least-squares Means. McRae, K., Ochsner, K.N., Mauss, I.B., Gabrieli, J.J.D., Gross, J.J., 2008. Gender differences in emotion regulation: an fMRI study of cognitive reappraisal. Gr. Process. Intergr. Relations 11, 143–162. https://doi.org/10.1177/1368430207088035. McRae, K., Gross, J.J., Weber, J., Robertson, E.R., Sokol-Hessner, P., Ray, R.D., Gabrieli, J.D.E., Ochsner, K.N., 2012. The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc. Cogn. Affect. Neurosci. 7, 11–22. https://doi.org/10.1093/scan/nsr093. Miller, G.A., Gration, G., Yee, C.M., 1988. Generalized implementation of an eye movement correction procedure. Psychophysiology 25, 241–243. https://doi.org/10. 1111/j.1469-8986.1988.tb00999.x. Moran, T.P., Jendrusina, A.A., Moser, J.S., 2013. The psychometric properties of the late positive potential during emotion processing and regulation. Brain Res. 1516, 66–75. https://doi.org/10.1016/j.brainres.2013.04.018. Morris, R.W., Sparks, A., Mitchell, P.B., Weickert, C.S., Green, M.J., 2012. Lack of corticolimbic coupling in bipolar disorder and schizophrenia during emotion regulation. Transl. Psychiatry 2, e90. https://doi.org/10.1038/tp.2012.16. Moser, J.S., Hajcak, G., Bukay, E., Simons, R.F., 2006. Intentional modulation of emotional responding to unpleasant pictures: an ERP study. Psychophysiology 43, 292–296. https://doi.org/10.1111/j.1469-8986.2006.00402.x. Nelson, B.D., Kessel, E.M., Jackson, F., Hajcak, G., 2016. The impact of an unpredictable context and intolerance of uncertainty on the electrocortical response to monetary gains and losses. Cogn. Affect. Behav. Neurosci. 16, 153–163. https://doi.org/10. 3758/s13415-015-0382-3. Oka, S., Chapman, C.R., Kim, B., Shimizu, O., Noma, N., Takeichi, O., Imamura, Y., Oi, Y., 2010. Predictability of painful stimulation modulates subjective and physiological responses. J. Pain 11, 239–246. https://doi.org/10.1016/j.jpain.2009.07.009. Parvaz, M.A., MacNamara, A., Goldstein, R.Z., Hajcak, G., 2012. Event-related induced frontal alpha as a marker of lateral prefrontal cortex activation during cognitive reappraisal. Cogn. Affect. Behav. Neurosci. 12, 730–740. https://doi.org/10.3758/ s13415-012-0107-9. Quoidbach, J., Berry, E.V., Hansenne, M., Mikolajczak, M., 2010. Positive emotion regulation and well-being: comparing the impact of eight savoring and dampening
strategies. Pers. Individ. Dif. 49, 368–373. https://doi.org/10.1016/j.paid.2010.03. 048. R Core Team, 2016. R: A Language and Environment for Statistical Computing. Raio, C.M., Orederu, T.A., Palazzolo, L., Shurick, A.A., Phelps, E.A., 2013. Cognitive emotion regulation fails the stress test. Proc. Natl. Acad. Sci. 110, 15139–15144. https://doi.org/10.1073/pnas.1305706110. Ray, R.D., McRae, K., Ochsner, K.N., Gross, J.J., 2010. Cognitive reappraisal of negative affect: converging evidence from EMG and self-report. Emotion 10, 587–592. https:// doi.org/10.1037/a0019015. Shermohammed, M., Mehta, P.H., Zhang, J., Brandes, C.M., Chang, L.J., Somerville, L.H., 2017. Does psychosocial stress impact cognitive reappraisal? Behavioral and neural evidence. J. Cogn. Neurosci. 29, 1803–1816. https://doi.org/10.1162/jocn_a_01157. Smoskia, M.J., Keng, S.L., Schiller, C.E., Minkei, J., Dichter, G.S., 2013. Neural mechanisms of cognitive reappraisal in remitted major depressive disorder. J. Affect. Disord. 151, 171–177. https://doi.org/10.1016/j.jad.2013.05.073. Speed, B.C., Jackson, F., Nelson, B.D., Infantolino, Z.P., Hajcak, G., 2017. Unpredictability increases the error-related negativity in children and adolescents. Brain Cogn. 119, 25–31. https://doi.org/10.1016/j.bandc.2017.09.006. Thiruchselvam, R., Blechert, J., Sheppes, G., Rydstrom, A., Gross, J.J., 2011. The temporal dynamics of emotion regulation: an EEG study of distraction and reappraisal. Biol. Psychol. 87, 84–92. https://doi.org/10.1016/j.biopsycho.2011.02.009. Thompson, L.A., Williams, K.L., L’Esperance, P.R., 2001. Context-dependent memory under stressful conditions: the case of skydiving. Hum. Factors J. Hum. Factors Ergon. Soc. 43, 611–619. https://doi.org/10.1518/001872001775870377. Visintainer, M., Colpicelli, J., Seligman, M., 1982. Tumor rejection in rats after inescapable or escapable shock. Science (80-.) 216, 437–439. https://doi.org/10.1126/ science.109924. Walker, S., O’Connor, D.B., Schaefer, A., 2011. Brain potentials to emotional pictures are modulated by alexithymia during emotion regulation. Cogn. Affect. Behav. Neurosci. 11, 463–475. https://doi.org/10.1021/la5017998. Wessa, M., Kanske, P., Neumeister, P., Bode, K., Heissler, J., Schönfelder, S., 2010. EmoPics: Subjektive und psychophysiologische Evaluationen neuen Bildmaterials für die klinisch-bio-psychologische Forschung [Subjective and psychophysiological evaluation of new picture stimuli for clinical-biopsychological research]. Z. Klin. Psychol. Psychother. 11.
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International Journal of Psychophysiology journal homepage: www.elsevier.com/locate/ijpsycho
Cognitive reappraisal in an unpredictable world: Prior context matters Michael J. Imburgio , Annmarie MacNamara ⁎
T
Department of Psychological and Brain Sciences, Texas A&M University, College Station, TX, USA
ARTICLE INFO
ABSTRACT
Keywords: Emotion regulation Late positive potential Event-related potential ERP LPP Unpredictability
Cognitive reappraisal is a higher order emotion regulation strategy, the effects of which can be measured using the late positive potential (LPP), an event-related potential that is larger for emotional versus neutral stimuli. Whereas the lab provides a relatively predictable and calm environment in which to engage in reappraisal, outside of the lab, individuals may need to enact reappraisal in unpredictable and anxiety-provoking environments. In prior work, unpredictable auditory tones have been shown to increase threat-processing and induce anxiety. Here, forty-seven participants performed a reappraisal task while being exposed in a blockwise fashion to a “Random Tone” sequence or silence (“No Tone”), to determine the effects of an unpredictable auditory stimulus on the reappraisal of negative pictures. In addition, exploratory analyses assessed whether starting block (i.e., beginning the task in a Random Tone versus No Tone block) would moderate effects. Results showed that during an early time window, reappraisal LPPs were smallest for participants who started in a No Tone block and who performed reappraisal in a No Tone block. Therefore, reappraisal may be optimally performed when conditions are predictable/calm, by participants whose initial learning context was also predictable/calm. In addition, larger LPPs for negative versus neutral images were only observed throughout the later portion of picture presentation for participants who began in a Random Tone block, suggesting that unpredictability may increase sustained attention towards aversive stimuli. The results fit within a growing body of work aimed at understanding contextual and individual differences in emotion regulation.
1. Introduction When implemented effectively, emotion regulation has mental, physical and social benefits (Denny and Ochsner, 2014; Haga et al., 2009; Quoidbach et al., 2010). On the other hand, difficulties implementing emotion regulation are associated with reduced psychological wellbeing and may play a role in the development and maintenance of disorders such as anxiety and depression (Campbell-Sills and Barlow, 2007). Over the past several years, cognitive reappraisal, an emotion regulation strategy that involves changing the meaning of a stimulus, has been studied extensively in the lab. For example, evidence suggests that when instructed to do so, both healthy and clinical samples can effectively down-regulate their response to emotional stimuli using reappraisal (McRae et al., 2008, 2012; Ray et al., 2010; Smoskia et al., 2013; but see Morris et al., 2012). In laboratory settings, reappraisal may be relatively straightforward. However, in the real world, reappraisal may be most needed in unpredictable, stress-inducing and distracting environments. Here, we sought to examine how an unpredictable context might compromise reappraisal, and whether individual differences in prior exposure to an unpredictable or calm context might modulate these effects. ⁎
Prior work has examined how stressful mood manipulations may affect subsequent attempts to reappraise. For example, Raio et al. (2013) asked participants to complete a threat-learning procedure in which they learned to associate one picture (a conditioned stimulus, CS +) with an aversive outcome but not another (CS−). Next, participants were trained in reappraisal and were explicitly instructed to reappraise the CS+. Twenty-four hours later, participants returned to the lab and were exposed to a physiological stressor (i.e., cold pressor test) or to a control condition, before completing the threat conditioning task again while employing their newly learned reappraisal skills. Results showed that the non-stressed group had reduced skin conductance responses to the CS+ following training in reappraisal, whereas the stressed group showed no such benefits (Raio et al., 2013). Therefore, an acute stressor may negatively affect participants' subsequent ability to implement reappraisal. On the other hand, however, some work has suggested that reappraisal is relatively resistant to stress. For example, Shermohammed et al. (2017) found that participants who underwent a psychosocial stressor (Trier Social Stress Test; Kirschbaum et al., 1993) showed no decrement in reappraisal ability, compared to participants in a control group. As such, evidence regarding the effect of stress on reappraisal has been mixed and results may depend on the type of stressor
Corresponding author at: Department of Psychological and Brain Sciences, Texas A&M University, 4235 TAMU, College Station, TX 77843, USA. E-mail address: [email protected] (M.J. Imburgio).
https://doi.org/10.1016/j.ijpsycho.2019.09.003 Received 27 February 2019; Received in revised form 30 August 2019; Accepted 9 September 2019 Available online 24 October 2019 0167-8760/ Published by Elsevier B.V.
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employed. Whereas a stressful event might have a downstream effect on participants' subsequent ability to engage in cognitive reappraisal, contextual manipulations that take place simultaneous with reappraisal might be more powerful. In prior work, irregular auditory tones have been used to induce an unpredictable context that participants find anxiety-provoking (Jackson et al., 2015; Nelson et al., 2016). In addition, listening to an unpredictable tone sequence while performing another task increases the electrocortical processing of errors (Jackson et al., 2015; Speed et al., 2017) and reduces electrocortical responses to reward (Nelson et al., 2016). Unpredictable tones have been found to increase attention towards threat and amygdala activation in humans, and to increase anxiety-like behaviors and amygdala activation in mice (Herry et al., 2007). However, it is currently unknown whether unpredictable tones might also impair cognitive regulation of negative and neutral stimuli. It is also possible that the extent to which an unpredictable context might interfere with participants' ability to reappraise stimuli might depend on an individual's prior experiences with that context. For example, participants in a study by Diener et al. (2009) completed a paradigm in which they were told that they could press a button to avoid electric shock. However, while this was true for some blocks of the experiment (controllable stress), there were other blocks in which participants were unable to escape electric shock, despite their best efforts (i.e., regardless of their button presses; uncontrollable stress). Results showed that prior experiences of controllability appeared to buffer or “immunize” participants against future experiences of uncontrollability (as measured by ERP component, post-imperative negative variation, PINV), whereas initial experiences of uncontrollability seemed to render individuals more vulnerable to future encounters with these situations. Both controllability and predictability can attenuate stress responding (Abbott et al., 1984; Geer et al., 1970; Oka et al., 2010; Visintainer et al., 1982) and controllability may in part exert its effects on stress by increasing the predictability of unpleasant events (Geer and Maisel, 1972); therefore, we reasoned that the initial conditions under which an individual first learns to perform a reappraisal task (i.e., no tone versus unpredictable tones) might affect his/her subsequent ability to reappraise stimuli under distracting or unpredictable conditions. Here, we examined the effect of context on reappraisal by asking participants to reappraise negative pictures while simultaneously listening to unpredictable tones or no tone (Jackson et al., 2015; Nelson et al., 2016). In addition to this within-subjects manipulation, we assigned participants to begin the task in an unpredictable or no tone block. We used an event-related potential, the late positive potential (LPP), to assess the effects of reappraisal on the processing of negative and neutral pictures. The LPP is a centroparietally maximal ERP component that begins around 300 ms following stimulus onset and is larger for emotional compared to neutral stimuli (Cuthbert et al., 2000). The LPP is smaller when participants are asked to reappraise the meaning of negative pictures (Blechert et al., 2012; Fitzgerald et al., 2016; Hajcak and Nieuwenhuis, 2006; Moran et al., 2013; Thiruchselvam et al., 2011, but see Babkirk et al., 2015; Decicco et al., 2014; Dennis and Hajcak, 2009; Walker et al., 2011), indicating reduced picture processing. Participants in the current study performed a well-validated reappraisal task commonly used with the LPP (Hajcak and Nieuwenhuis, 2006), in which they were asked to reappraise or watch negative pictures, as well as to passively view neutral pictures. We hypothesized that negative pictures would elicit larger LPPs than neutral pictures, and that reappraisal would reduce the LPP to negative pictures. Additionally, we hypothesized that reappraisal would be less effective at modulating the LPP during unpredictable tone blocks compared to blocks on which no tone was presented. We also examined an exploratory hypothesis that participants who began with a no tone block might be less affected by the tones, as evidenced by reappraisal's effect on the LPP (Diener et al., 2009).
2. Method 2.1. Participants Sample size was determined by our a priori decision to run the study for a single semester, with the total N resulting from the number of undergraduates who signed up to complete the study during this time. The sample consisted of 54 undergraduates who completed the study for course credit. Seven participants were eliminated from analyses due to excessive artifacts during EEG recordings (i.e., on > 50% of trials), leaving a final sample of 47 participants (57% female, 41% male, 2% other; MAGE = 19.04 years; SD = 3.31). Study procedures were in compliance with the Helsinki Declaration of 1975 (as revised in 1983) and were approved by the Texas A&M University institutional review board. 2.2. Stimuli One hundred negative and 50 neutral pictures were selected from the International Affective Picture System (IAPS; Lang et al., 2008) and the Emotional Picture Set (EmoPicS; Wessa et al., 2010). The auditory tone sequence presented in some blocks was identical to that used in previous work (Herry et al., 2007; Jackson et al., 2015; Nelson et al., 2016). The random tones were generated by starting with a regular tone sequence (for which the carrier frequency was 100 Hz, pulse duration was 40 ms, and mean pulse spacing was 200 ms), then applying a random temporal shift to each tone in the regular sequence. The resulting random tones were presented to participants through headphones at 90 dB. 2.3. Reappraisal task The reappraisal task was modeled after those previously used (Hajcak and Nieuwenhuis, 2006; Moser et al., 2006); however, during some blocks, a random tone (described above) was played over headphones, while in other blocks no tone was played. At the beginning of the experiment, participants were trained in the reappraisal task. They were told that they would be viewing negative and neutral pictures and that negative pictures would be preceded by the word “WATCH” or “DECREASE” and neutral pictures would be preceded by the word “VIEW”. Participants were told that when they saw the word “WATCH” or “VIEW”, that they should simply view the picture as they normally would, without trying to change their response in any way. However, participants were instructed that when they saw the word “DECREASE” before presentation of a negative picture, they should try to reduce their emotional response to the picture by changing its meaning. For example, if viewing a picture of a house fire, participants could tell themselves that help was on the way and everyone would survive, or for a photo of a gruesome war scene, they could tell themselves that the picture was taken from a movie and no one was really hurt. Participants viewed negative pictures and the experimenter provided examples of how participants could reappraise those pictures. Following this, participants completed five practice trials to become familiar with the paradigm. After each practice picture that had been preceded by the word “DECREASE”, the experimenter asked the participant how they had attempted to reduce their emotional response and provided guidance or feedback as necessary (i.e., to ensure participants understood directions and were using cognitive reappraisal; Parvaz et al., 2012). Once they had been trained in and had practiced the reappraisal task, participants were told that they would also hear some tones played over headphones during some portions of the experiment and that these tones were unrelated to their task. Following these instructions, participants completed the task while continuous electroencephalography (EEG) was recorded. The task was broken into six blocks – three blocks in which participants listened to a random sequence of tones throughout the entire block (“Random 174
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condition (No Tone, Random Tone) on the LPP were examined using mixed linear models in which picture condition, tone condition and starting block were fixed factors and participant was a random factor. Analyses were performed separately for each LPP time window. Linear models were fit using the lme4 package (Bates et al., 2008) with p values estimated using the lmerTest package (Kuznetsova et al., 2017). When necessary, significant interactions were followed up by comparisons of estimated marginal means with Bonferroni-corrected p-values using the emmeans package (Lenth and Herve, 2018). We chose to examine these effects using mixed linear models rather than mixed between-within ANOVAs because they allowed us to formally test whether the inclusion of the starting block factor and associated interaction terms accounted for a significant proportion of variance. We began with a model including the fixed factors, picture condition and tone condition, their interaction term, and random factor, participant. We then tested whether introducing the fixed factor, starting block and all associated interaction terms to the model accounted for a significant proportion of additional variance using a maximum likelihood ratio test. To account for the exploratory nature of these tests and given that we had already performed one set of tests, we used a more stringent significance threshold of p = .05/2 = .025. Theoretically, mixed linear models can also better account for unequal group sizes (i.e., in each level of the starting block factor; Bagiella et al., 2000). In addition, the lmerTest and emmeans packages use the Satterthwaite method of estimating degrees of freedom, which does not assume equal variances across groups, better models heterogeneity among groups and subjects, and better controls for Type I error in the case of mixed models when compared to a traditional residual df approximation (Keselman et al., 1999). Nonetheless, it should be noted that using mixed between-within ANOVAs that were GreenhouseGeisser corrected for violations of sphericity yielded conclusions in line with those presented here.
Tone”) and three blocks in which no tones were played (“No Tone”). Trials were also blocked by picture type; this resulted in one neutral, two negative Random Tone blocks and one neutral, two negative No Tone blocks, each containing 25 trials. Participants were informed about the picture type at the beginning of each block (e.g., “In this block you will see only negative pictures”). An even number of “WATCH”, “REAPPRAISE” and “VIEW” trials were presented in Random Tone and No Tone blocks and trials were presented in random order. Therefore, there were 150 trials in total: 25 No Tone “VIEW” neutral trials; 25 random tone “VIEW” neutral trials; 25 no tone “WATCH” negative trials; 25 random tone “WATCH” negative trials; 25 no tone “REAPPRAISE” negative trials and 25 random tone “REAPPRAISE” negative trials. Each trial began with a 2000 ms presentation of the word, “VIEW” (for neutral trials), “WATCH” (for passive viewing negative trials), or “DECREASE” (for reappraise negative trials). Next, participants viewed a white fixation cross on a black background for 500 ms; this was followed by a negative or neutral picture that was presented for 6000 ms. Each trial was separated by a white fixation cross presented on a black background for 2000–2500 ms. Pictures were randomly selected from the neutral and negative picture sets and each picture was shown exactly once during the task. Participants were randomized to begin with either a No Tone (N = 21) or Random Tone (N = 26) block and block order was randomized across the remainder of trials for each participant. 2.4. EEG recording and processing Continuous EEG was recorded using an ActiCap and the ActiChamp amplifier (Brain Products, Gilching Germany). Thirty-two electrode sites were used based on the 10/20 system. The electrooculogram (EOG) was recorded from four facial electrodes: two electrodes were placed approximately 1 cm above and below the right eye, forming a bipolar channel to measure vertical eye movement and blinks and two electrodes were placed approximately 1 cm beyond the outer edge of each eye, forming a bipolar channel to measure horizontal eye movements. EEG data was digitized at a 24-bit resolution with a sampling rate of 500 Hz. EEG data were processed offline using BrainVision Analyzer 2 software (Brain Products GmbH, Gilching, Germany). Data were segmented for each trial beginning 200 ms before picture onset and lasting for 6200 ms (i.e., for the entire picture duration). The signal from each electrode was referenced offline to the average of the left and right mastoids (TP9/10) and band-pass filtered with high-pass and low-pass filters of 0.01 and 30 Hz, respectively. Eye blink and ocular corrections used the method developed by Miller et al. (1988). Artifact analysis was used to identify a voltage step of > 50.0 μV between sample points, a voltage difference of 300.0 μV within a trial, and a maximum voltage difference of < 0.50 μV within 100-ms intervals. Trials were also inspected visually for any remaining artifacts, and data from individual channels containing artifacts were rejected on a trial-to-trial basis. The number of retained trials did not differ by condition, F(5,276) = 0.18, p = .97 (Random Tone, Neutral View M = 23.68, SD = 1.85; Random Tone, Negative Watch M = 23.68, SD = 1.78; Random Tone, Negative Reappraise M = 23.68, SD = 2.00; No Tone, Neutral View M = 23.92, SD = 1.40; No Tone, Negative Watch M = 23.50, SD = 1.95; No Tone, Negative Reappraise M = 23.70, SD = 2.07; Min = 14, Max = 25). The LPP was scored by averaging amplitudes from three frontocentral sites at which it was maximal (FC1, FC2, and Cz), during an early time window (400–3200 ms) and a late time window (3200–6000 ms).
3. Results Grand-average waveforms for each combination of picture and tone condition are presented in Fig. 1. Headmaps corresponding to the voltage difference for Negative Watch minus Neutral View and Negative Reappraise minus Neutral View are also shown in Fig. 1. Fig. 2 depicts grand-average waveforms for each condition, shown separately for Random Tone blocks and No Tone blocks. Table 1 presents mean amplitudes at the frontocentral pooling for the early and late time windows, shown separately for each picture and tone condition as well as each starting block. 3.1. LPP (400–3200 ms) The inclusion of the starting block factor accounted for a significant proportion of variance beyond that accounted for by the model including only picture condition and tone condition, χ2(6) = 25.11, p < .001; therefore, only results from the full model are reported below. Significant main effects of picture condition, F(2,225) = 31.45, p < .001 (Negative Watch > Neutral View, t[225] = 6.65, p < .001, β = 0.58; Negative Reappraise > Neutral View, t[225] = 7.07, p < .001, β = 0.62; Negative Watch vs. Negative Reappraise, t [225] = 0.43, p = 1.00), starting block X picture condition, F (2,225) = 4.16, p = .02 (Random Tone first, Negative Reappraise > No Tone First, Negative Reappraise, t[45] = 2.37, p = .02, β = 0.60; Random Tone first, Negative Watch vs. No Tone first, Negative Watch, p = .07; Random Tone first, Neutral View vs. No Tone first, Neutral View, p = .47) and starting block X tone condition, F(2,225) = 5.14, p = .02 (Random Tone first, No Tone Block > No Tone First, No Tone Block, t[45] = 2.51, p = .02, β = 0.56; Random Tone first, Random Tone Block vs. No Tone first, Random Tone Block, p = .26) were qualified by a three-way interaction between starting block X picture condition X tone condition, F(2,225) = 4.11, p = .02. Follow-up tests
2.5. Data analyses Data analyses were conducted using R version 3.5.1 (R Core Team, 2016). The effects of picture condition (Netural View, Negative Watch, Negative Reappraise), starting block (No Tone, Random Tone) and tone 175
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Fig. 1. Grand-average waveforms depict amplitudes at the frontocentral pooling where the LPP was scored, shown separately for each condition; the vertical dashed line denotes the end of the early time window and the beginning of the late time window. Headmaps show the spatial distribution of voltage differences for Negative Watch minus Neutral View trials (top) and Negative Reappraise minus Neutral View trials (bottom), shown separately for each time window in which the LPP was scored. Shaded areas depict pooled SEM of the groups across both windows.
Fig. 2. Grand-average waveforms depict amplitudes at the frontocentral pooling where the LPP was scored, shown separately for each picture condition and group in No Tone blocks (top) and Random Tone blocks (bottom); the vertical dashed line denotes the end of the early time window and the beginning of the late time window. Shaded areas depict pooled SEM of the groups across both windows.
performed separately within each picture condition1 revealed a significant starting block X tone condition interaction within Negative Reappraise, F(1,45) = 16.65, p < .001, but not within Negative Watch (p = .94) or Neutral View (p = .83). Follow-up tests revealed that No Tone first, No Tone Reappraise was smaller than the other three Reappraisal cells (Table 1). The results of these tests were as follows: Random Tone first, No Tone Reappraise > No Tone first, No Tone Reappraise, t(43.16) = 3.58, p < .001, β = 0.94; Random Tone first,
Random Tone reappraise > No Tone first, No Tone Reappraise, t (37.77) = 3.29, p = .002, β = 0.89; No Tone first, Random Tone reappraise > No Tone first, No Tone Reappraise, t(20) = 5.31, p < .001, β = 0.68. There were no differences between the other three cells (all ps > .26). No other effects reached significance in the full model, ps > .06. 3.2. LPP (3200–6000 ms) The inclusion of the starting block factor accounted for a significant proportion of variance beyond that accounted for by the model including only picture condition and tone condition, χ2(6) = 16.21, p = .01; therefore, only results from the full model are reported below. A main effect of picture condition, F(2,225) = 11.45, p < .001, was qualified by a two-way interaction between starting block X picture condition, F(2,225) = 4.05, p = .02, which showed that negative pictures elicited larger LPPs than neutral pictures for participants that had started with a Random Tone block (main effect of picture condition, F
1
Another way to interpret this interaction would have been to compare picture conditions separately within each tone condition. For example, this might have revealed that reappraisal reduced the LPP in one tone condition but not the other. For participants that completed a No Tone block first, the difference between Negative Reappraise and Negative Watch trials did not reach significance within No Tone blocks (p = .35, β = 0.34) or within Random Tone blocks (p = .12, β = 0.33). Nonetheless, condition means were in opposite directions: Negative Watch > Negative Reappraise in the No Tone blocks and Negative Reappraise > Negative Watch in the Random Tone blocks. 176
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Table 1 Means (standard deviations) for the LPP, shown separately for each time window, condition and group. Early window (400–3200 ms)
Neutral view Negative watch Negative reappraise
Late window (3200–6000 ms)
Random tone block first
No tone block first
Random tone (μv)
No tone (μv)
Random tone (μv)
1.89 (3.94) 6.42 (5.49) 6.29 (4.54)
2.07 (3.60) 6.43 (6.77) 7.28 (5.78)
1.16 (6.40) 3.30 (6.32) 5.37 (5.75)
Random tone block first
No tone block first
No tone (μv)
Random tone (μv)
No tone (μv)
Random tone (μv)
No tone (μv)
1.07 (4.57) 3.20 (6.67) 1.25 (5.71)
1.82 (3.94) 7.55 (5.17) 4.64 (4.66)
2.75 (4.21) 6.97 (5.59) 6.41 (6.56)
2.31 (8.50) 2.90 (8.57) 4.79 (8.53)
1.89 (5.66) 3.64 (10.86) 2.20 (9.36)
served as contextual conditioning for learning that took place throughout this first block. That is, although we trained participants on cognitive reappraisal before they began the task, participants' skill and comfort level with the task likely continued to increase throughout the first block. If learning took place during the first block in the absence of unpredictable tones, this might explain why participants were more likely to experience interference during subsequently presented unpredictable blocks. Taken as context-dependent learning, the effects of the current study are in line with prior work that asked participants to encode and recall information either in a stressful context (while skydiving) or a calm context (on the ground; Thompson et al., 2001). Results showed that, for participants who learned information under calm conditions, a stressful context decreased performance compared to a calm context. On the other hand, for participants who learned information while skydiving, recall was poor independent of retrieval context. Therefore, as in the current study, participants who learned in a calm context were selectively sensitive to the subsequent introduction of a stressful context, whereas a stressful context during learning hindered performance more broadly. As such, the current results support the notion that affect plays a role in cognitive control. Moreover, our results suggest a role for historical affective context. That is, either a current or historical unpredictable context appears to compromise reappraisal, as compared to reappraisal as it is typically performed in the lab (i.e., free from auditory tones). Nonetheless, we caution that other, non-affective mechanisms might also explain the current results. That is, in addition to inducing stress or anxiety, the unpredictable tones might have been distracting – perhaps especially for participants who first acclimated to the task in the absence of the tones. In keeping with this, prior work found that individuals who had been exposed to a less distracting context were more susceptible to the effects of distraction during subsequent task performance than individuals who had previously been exposed to a noisy or distracting context. Additionally, participants who were accustomed to distracting contexts experienced generalized performance deficits independent of future distractions (Heft, 1979). Furthermore, biased competition models of attention suggest that distraction most often interferes with cognitive tasks that rely heavily on the frontal lobe (Lavie, 2005), such as cognitive reappraisal (see Buhle et al., 2014), which could explain why we observed interference for the reappraisal condition in particular. During the later portion of picture presentation, negative pictures ceased to elicit an increased LPP for participants who had begun the task with a toneless block. On the other hand, participants who were first exposed to the unpredictable tone sequence continued to show larger LPPs for negative compared to neutral images throughout the later portion of picture presentation. Prior work suggests that unpredictable tone sequences may increase participants' attention towards aversive stimuli. For example, while listening to unpredictable tones, participants were more likely to orient towards angry faces rather than neutral faces (Herry et al., 2007) and to show increased electrocortical processing of errors, which can be viewed as internal threats (Jackson et al., 2015). Therefore, individuals who began the task in the unpredictable tone condition may have learned to engage more with the
[2,128] = 18.03, p < .001, Negative Reappraise versus Neutral View, t [128] = 3.86, p < .001, β = 0.59; Negative Watch versus Neutral View, t[128] = 5.91, p < .001, β = 0.92; Negative Watch versus Negative Reappraise, p = .10), but not for participants who had started with a No Tone block (main effect of picture condition, p = .38). No other effects reached significance in the full model, ps > .10. 4. Discussion Cognitive reappraisal is a complex, higher-order emotion regulation strategy that relies on an orchestrated set of mental operations and may be vulnerable to interference from contextual factors. Work examining the effect of stress manipulations on cognitive reappraisal has yielded mixed results (Raio et al., 2013; Shermohammed et al., 2017). However, no work to date has examined how unpredictability might modulate reappraisal's effects on neural activity, or how an individual's history with an unpredictable context might affect reappraisal. Here, we examined the effect of a random auditory tone (versus no tone) on the reappraisal of negative images, as measured by the LPP. Results showed that early reappraisal LPPs were smallest for participants who started in a No Tone block and who performed reappraisal in a No Tone block. Therefore, reappraisal may be optimally performed when conditions are predictable/calm, by participants whose initial learning context was also predictable/calm. In addition, whereas negative pictures elicited larger LPPs than neutral pictures across all participants in the early time window, only participants who began the experiment in a Random Tone block showed larger LPPs to negative compared to neutral pictures, in the late time window. This pattern of results suggests that initial exposure to an unpredictable context might increase the sustained processing of negative stimuli. Given that both predictability and controllability can attenuate physiological stress responding (Abbott et al., 1984; Geer et al., 1970; Oka et al., 2010; Visintainer et al., 1982), we had expected that beginning the task in the no tone condition might protect participants from their deleterious effects on reappraisal. This hypothesis was based on the work of Diener et al. (2009), who found that participants who began a task with control over shock exposure showed more normative electrocortical responding than participants who began the study with no control over the shock (Diener et al., 2009). Here, results differed, in that participants who had started in a No Tone block were most affected by the unpredictable tones, showing larger early reappraisal LPPs (compared to the No Tone condition). Task differences may in part explain divergence between the current results and prior findings. First, despite their similarities, uncontrollability and unpredictability are distinct phenomena and may elicit dissociable effects (Baker and Stephenson, 2000). Second, in the current study, unpredictable tones were unrelated to participants' task, which was to reappraise pictures. By contrast, in Diener et al. (2009), controllability was central to and in line with the task instructions, in which participants were told that they could press a button to avoid shock delivery. Therefore, an initial experience of controllability in the Diener study may have reinforced participants' sense of self-efficacy and belief in the task instructions. Here, the tone condition during participants' starting block may have 177
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aversive or threatening aspects of pictures, leading to prolonged processing of negative pictures throughout the study. Reappraisal of negative images did not significantly reduce the LPP, irrespective of starting block or tone condition. Though not in line with our prediction, these results are in accordance with several other studies that have also failed to observe a reduction in the LPP following reappraisal (Babkirk et al., 2015; Decicco et al., 2014; Dennis and Hajcak, 2009; Walker et al., 2011). One possibility is that reappraisal is more difficult for some pictures than others, such as those that are highly arousing (Langeslag and Surti, 2017); as such, reappraisal may have been more effective on some trials than others, reducing the effect size across the experiment. Additionally, reappraisal is a cognitively demanding technique: individuals must rapidly generate an alternative explanation for a stimulus and then must sustain and elaborate on this explanation throughout the duration of stimulus presentation. Therefore, individual variability in the implementation of this technique is to be expected; moreover, changing contexts and unpredictable tones may have made our task particularly challenging. Nonetheless, we note that although reappraisal did not significantly reduce the LPP across participants, individuals who began the task in the No Tone condition showed descriptively smaller LPPs during reappraisal compared to passive viewing of negative pictures. The next generation of emotion regulation research is likely to include a focus on understanding individual differences in emotion regulation, particularly as they pertain to emotion regulation that takes place outside of the lab. Ironically, reappraisal may be most needed in unpredictable or stressful situations, yet it may typically be first introduced in a predictable and safe environment, such as a therapist's office (e.g., in cognitive therapy). In order to help reappraisal skills generalize, future work may wish to examine how best to prepare individuals to reappraise in unpredictable environments. Additionally, a better understanding of the mechanisms underlying contextual effects on reappraisal is needed, including accounting for the potential contributions of anxiety, stress, and distraction. While the random tones employed in the current work have previously been found to invoke anxiety and orienting towards aversive stimuli (Jackson et al., 2015; Nelson et al., 2016), a limitation of the current study is that we did not have subjective ratings to determine whether the tones led to increased anxiety during reappraisal. Similarly, the current work relied solely on the LPP to assess reappraisal's effects on picture processing. Therefore, future work might wish to include subjective picture ratings and to assess associations between these ratings and the LPP. Finally, we used a no tone control condition because we thought that even predictable tones might interfere with a demanding cognitive task like reappraisal. If, however, similar effects were observed using predictable tones as a control condition, this might help rule out distraction or other non-specific effects as a potential explanation. Although the no tone control condition was likely more predictable than the random tones condition, it might not constitute a purely predictable context. Future work might wish to examine the effects of introducing a predictable context on reappraisal ability. In sum, previous work has examined cognitive reappraisal independent of context, even though context likely has a great effect on an individual's ability to regulate their emotions (Aldao, 2013). The results presented here suggest that an individual's prior experience may moderate the effect of context on emotion regulation. As such, the current work provides a means of understanding individual variation in reappraisal ability, and serves as groundwork for future work aimed at tailoring emotion regulation training and strategy to the individual.
References Abbott, B.B., Schoen, L.S., Badia, P., 1984. Predictable and unpredictable shock: behavioral measures of aversion and physiological measures of stress. Psychol. Bull. 96, 45–71. https://doi.org/10.1037/0033-2909.96.1.45. Aldao, A., 2013. The future of emotion regulation research: capturing context. Perspect. Psychol. Sci. 8, 155–172. https://doi.org/10.1177/1745691612459518. Babkirk, S., Rios, V., Dennis, T.A., 2015. The late positive potential predicts emotion regulation strategy use in school-aged children concurrently and two years later. Dev. Sci. 18, 832–841. https://doi.org/10.1111/desc.12258. Bagiella, E., Sloan, R.P., Heitjan, D.F., 2000. Mixed-effects models in psychophysiology mixed-effects models in psychophysiology. Psychophysiology 14, 13–20. Baker, S.R., Stephenson, D., 2000. Prediction and control as determinants of behavioural uncertainty: effects on task performance and heart rate reactivity. Integrative Physiological and Behavioral Science. https://doi.org/10.1007/BF02688786. Bates, D., Maechler, M., Dai, B., 2008. The lme4 Package, version 0.999375-26. http:// cran.r-project.org. Blechert, J., Sheppes, G., Tella, C., Williams, H., Gross, J.J., 2012. See what you think: reappraisal modulates behavioral and neural responses to social stimuli. Psychol. Sci. 23, 346–353. https://doi.org/10.1177/0956797612438559. Buhle, J.T., Silvers, J.A., Wage, T.D., Lopez, R., Onyemekwu, C., Kober, H., Webe, J., Ochsner, K.N., 2014. Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb. Cortex 24, 2981–2990. https://doi.org/10.1093/ cercor/bht154. Campbell-Sills, L., Barlow, D.H., 2007. Incorporating emotion regulation into conceptualizations and treatments of anxiety and mood disorders, Handbook of Emotion Regulation. The Guilford Press, New York, NY. Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., Lang, P.J., 2000. Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol. Psychol. 52, 95–111. https://doi.org/10.1016/S0301-0511(99) 00044-7. Decicco, J.M., Otoole, L.J., Dennis, T.A., 2014. The late positive potential as a neural signature for cognitive reappraisal in children. Dev. Neuropsychol. 39, 497–515. https://doi.org/10.1080/87565641.2014.959171. Dennis, T.A., Hajcak, G., 2009. The late positive potential: a neurophysiological marker for emotion regulation in children. J. Child Psychol. Psychiatry Allied Discip. 50, 1373–1383. https://doi.org/10.1111/j.1469-7610.2009.02168.x. Denny, B.T., Ochsner, K.N., 2014. Behavioral effects of longitudinal training in cognitive reappraisal. Emotion 14, 425–433. https://doi.org/10.1037/a0035276. Diener, C., Struve, M., Balz, N., Kuehner, C., Flor, H., 2009. Exposure to uncontrollable stress and the postimperative negative variation (PINV): prior control matters. Biol. Psychol. 80, 189–195. https://doi.org/10.1016/j.biopsycho.2008.09.002. Fitzgerald, J.M., MacNamara, A., DiGangi, J.A., Kennedy, A.E., Rabinak, C.A., Patwell, R., Greenstein, J.E., Proescher, E., Rauch, S.A.M., Hajcak, G., Phan, K.L., 2016. An electrocortical investigation of voluntary emotion regulation in combat-related posttraumatic stress disorder. Psychiatry Res. - Neuroimaging 249, 113–121. https:// doi.org/10.1016/j.pscychresns.2015.12.001. Geer, J.H., Maisel, E., 1972. Evaluating the effects of the prediction-control confound. J. Pers. Soc. Psychol. 23, 314–319. https://doi.org/10.1037/h0033122. Geer, J.H., Davison, G.C., Gatchel, R.I., 1970. Reduction of stress in humans through nonveridical perceived control of aversive stimulation. J. Pers. Soc. Psychol. 16, 731–738. https://doi.org/10.1037/h0030014. Haga, S.M., Kraft, P., Corby, E.K., 2009. Emotion regulation: antecedents and well-being outcomes of cognitive reappraisal and expressive suppression in cross-cultural samples. J. Happiness Stud. 10, 271–291. https://doi.org/10.1007/s10902-007-9080-3. Hajcak, G., Nieuwenhuis, S., 2006. Reappraisal modulates the electrocortical response to unpleasant pictures. Cogn. Affect. Behav. Neurosci. 6, 291–297. https://doi.org/10. 3758/CABN.6.4.291. Heft, H., 1979. Background and focal environmental conditions of the home and attention in young children. J. Appl. Soc. Psychol. 9, 47–69. https://doi.org/10.1111/j.15591816.1979.tb00794.x. Herry, C., Bach, D.R., Esposito, F., Di Salle, F., Perrig, W.J., Scheffler, K., Luthi, A., Seifritz, E., 2007. Processing of temporal unpredictability in human and animal amygdala. J. Neurosci. 27, 5958–5966. https://doi.org/10.1523/JNEUROSCI.521806.2007. Jackson, F., Nelson, B.D., Proudfit, G.H., 2015. In an uncertain world, errors are more aversive: evidence from the error-related negativity. Emotion 15, 12–16. https://doi. org/10.1037/emo0000020. Keselman, H.J., Kowalchuk, R.K., Algina, J., Wolfinger, R.D., 1999. The analysis of repeated measurements: a comparison of mixed-model Satterthwaite F tests and a nonpooled adjusted degrees of freedom multivariate test. Commun. Stat. - Theory Methods. https://doi.org/10.1080/03610929908832460. Kirschbaum, C., Pirke, K.M., Hellhammer, D.H., 1993. The ‘Trier Social Stress Test’–a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76–81. https://doi.org/10.1159/000119004. Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., 2017. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82. https://doi.org/10.18637/jss.v082. i13. Lang, P.J., Bradley, M.M., Cuthbert, B.N., 2008. International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual (Rep. No. A-8). (Gainsville, FL). Langeslag, S.J.E., Surti, K., 2017. The effect of arousal on regulation of negative emotions using cognitive reappraisal: an ERP study. Int. J. Psychophysiol. 118, 18–26. https:// doi.org/10.1016/j.ijpsycho.2017.05.012. Lavie, N., 2005. Distracted and confused?: selective attention under load. Trends Cogn.
Acknowledgements Thanks to Blake Barley for his assistance in data collection and processing. Thanks to Greg Hajcak for providing the unpredictable tone sequence. Annmarie MacNamara is supported by National Institute of Mental Health grant, K23MH105553. 178
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M.J. Imburgio and A. MacNamara Sci. https://doi.org/10.1016/j.tics.2004.12.004. Lenth, R.L., Herve, M., 2018. Emmeans: Estimated Marginal Means, aka Least-squares Means. McRae, K., Ochsner, K.N., Mauss, I.B., Gabrieli, J.J.D., Gross, J.J., 2008. Gender differences in emotion regulation: an fMRI study of cognitive reappraisal. Gr. Process. Intergr. Relations 11, 143–162. https://doi.org/10.1177/1368430207088035. McRae, K., Gross, J.J., Weber, J., Robertson, E.R., Sokol-Hessner, P., Ray, R.D., Gabrieli, J.D.E., Ochsner, K.N., 2012. The development of emotion regulation: an fMRI study of cognitive reappraisal in children, adolescents and young adults. Soc. Cogn. Affect. Neurosci. 7, 11–22. https://doi.org/10.1093/scan/nsr093. Miller, G.A., Gration, G., Yee, C.M., 1988. Generalized implementation of an eye movement correction procedure. Psychophysiology 25, 241–243. https://doi.org/10. 1111/j.1469-8986.1988.tb00999.x. Moran, T.P., Jendrusina, A.A., Moser, J.S., 2013. The psychometric properties of the late positive potential during emotion processing and regulation. Brain Res. 1516, 66–75. https://doi.org/10.1016/j.brainres.2013.04.018. Morris, R.W., Sparks, A., Mitchell, P.B., Weickert, C.S., Green, M.J., 2012. Lack of corticolimbic coupling in bipolar disorder and schizophrenia during emotion regulation. Transl. Psychiatry 2, e90. https://doi.org/10.1038/tp.2012.16. Moser, J.S., Hajcak, G., Bukay, E., Simons, R.F., 2006. Intentional modulation of emotional responding to unpleasant pictures: an ERP study. Psychophysiology 43, 292–296. https://doi.org/10.1111/j.1469-8986.2006.00402.x. Nelson, B.D., Kessel, E.M., Jackson, F., Hajcak, G., 2016. The impact of an unpredictable context and intolerance of uncertainty on the electrocortical response to monetary gains and losses. Cogn. Affect. Behav. Neurosci. 16, 153–163. https://doi.org/10. 3758/s13415-015-0382-3. Oka, S., Chapman, C.R., Kim, B., Shimizu, O., Noma, N., Takeichi, O., Imamura, Y., Oi, Y., 2010. Predictability of painful stimulation modulates subjective and physiological responses. J. Pain 11, 239–246. https://doi.org/10.1016/j.jpain.2009.07.009. Parvaz, M.A., MacNamara, A., Goldstein, R.Z., Hajcak, G., 2012. Event-related induced frontal alpha as a marker of lateral prefrontal cortex activation during cognitive reappraisal. Cogn. Affect. Behav. Neurosci. 12, 730–740. https://doi.org/10.3758/ s13415-012-0107-9. Quoidbach, J., Berry, E.V., Hansenne, M., Mikolajczak, M., 2010. Positive emotion regulation and well-being: comparing the impact of eight savoring and dampening
strategies. Pers. Individ. Dif. 49, 368–373. https://doi.org/10.1016/j.paid.2010.03. 048. R Core Team, 2016. R: A Language and Environment for Statistical Computing. Raio, C.M., Orederu, T.A., Palazzolo, L., Shurick, A.A., Phelps, E.A., 2013. Cognitive emotion regulation fails the stress test. Proc. Natl. Acad. Sci. 110, 15139–15144. https://doi.org/10.1073/pnas.1305706110. Ray, R.D., McRae, K., Ochsner, K.N., Gross, J.J., 2010. Cognitive reappraisal of negative affect: converging evidence from EMG and self-report. Emotion 10, 587–592. https:// doi.org/10.1037/a0019015. Shermohammed, M., Mehta, P.H., Zhang, J., Brandes, C.M., Chang, L.J., Somerville, L.H., 2017. Does psychosocial stress impact cognitive reappraisal? Behavioral and neural evidence. J. Cogn. Neurosci. 29, 1803–1816. https://doi.org/10.1162/jocn_a_01157. Smoskia, M.J., Keng, S.L., Schiller, C.E., Minkei, J., Dichter, G.S., 2013. Neural mechanisms of cognitive reappraisal in remitted major depressive disorder. J. Affect. Disord. 151, 171–177. https://doi.org/10.1016/j.jad.2013.05.073. Speed, B.C., Jackson, F., Nelson, B.D., Infantolino, Z.P., Hajcak, G., 2017. Unpredictability increases the error-related negativity in children and adolescents. Brain Cogn. 119, 25–31. https://doi.org/10.1016/j.bandc.2017.09.006. Thiruchselvam, R., Blechert, J., Sheppes, G., Rydstrom, A., Gross, J.J., 2011. The temporal dynamics of emotion regulation: an EEG study of distraction and reappraisal. Biol. Psychol. 87, 84–92. https://doi.org/10.1016/j.biopsycho.2011.02.009. Thompson, L.A., Williams, K.L., L’Esperance, P.R., 2001. Context-dependent memory under stressful conditions: the case of skydiving. Hum. Factors J. Hum. Factors Ergon. Soc. 43, 611–619. https://doi.org/10.1518/001872001775870377. Visintainer, M., Colpicelli, J., Seligman, M., 1982. Tumor rejection in rats after inescapable or escapable shock. Science (80-.) 216, 437–439. https://doi.org/10.1126/ science.109924. Walker, S., O’Connor, D.B., Schaefer, A., 2011. Brain potentials to emotional pictures are modulated by alexithymia during emotion regulation. Cogn. Affect. Behav. Neurosci. 11, 463–475. https://doi.org/10.1021/la5017998. Wessa, M., Kanske, P., Neumeister, P., Bode, K., Heissler, J., Schönfelder, S., 2010. EmoPics: Subjektive und psychophysiologische Evaluationen neuen Bildmaterials für die klinisch-bio-psychologische Forschung [Subjective and psychophysiological evaluation of new picture stimuli for clinical-biopsychological research]. Z. Klin. Psychol. Psychother. 11.
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