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Articles, Behavioral/Cognitive

Training the Emotional Brain: Improving Affective Control through Emotional Working Memory Training

Susanne Schweizer, Jessica Grahn, Adam Hampshire, Dean Mobbs and Tim Dalgleish
Journal of Neuroscience 20 March 2013, 33 (12) 5301-5311; https://doi.org/10.1523/JNEUROSCI.2593-12.2013
Susanne Schweizer
1Medical Research Council Cognition and Brain Sciences Unit, Cambridge, CB2 7EF, United Kingdom, and
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Jessica Grahn
2Western University, Brain Mind Institute and Department of Psychology, Natural Sciences Centre, London, Ontario, N6A 5B7, Canada
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Adam Hampshire
2Western University, Brain Mind Institute and Department of Psychology, Natural Sciences Centre, London, Ontario, N6A 5B7, Canada
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Dean Mobbs
1Medical Research Council Cognition and Brain Sciences Unit, Cambridge, CB2 7EF, United Kingdom, and
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Tim Dalgleish
1Medical Research Council Cognition and Brain Sciences Unit, Cambridge, CB2 7EF, United Kingdom, and
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  • Figure 1.
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    Figure 1.

    A, Task design of the eWM training (dual n-back) task for a sample training block where n-back = 1. Stimuli with a bold pink border represent target stimuli for the current block. Participants respond with a button press if the target stimulus in either or both modalities matches the stimulus n positions back. In this n-back = 1 example, there is a match because, for the visuospatial modality, the current face appears in the same location as the face 1-position back; and for the auditory target, the word (RAPE) is the same as the word one-back. B, C, Task-demand-related BOLD activation that was observed comparing conditions of lower task-demand (n-back = 1) and higher task-demand (n-back = 3) at pre-training. All reported BOLD activation was significantly different across these conditions at the whole-brain level, with significance levels corrected for false discovery rates at PFDR < 0.05. Activation increases (B) and activation decreases (C) in condition n-back = 3 compared with n-back = 1. For a full overview of differential activation, see Table 1. Error bars indicate SEM.

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    Figure 2.

    A, The graph represents mean performance accuracy on target trials at the levels of n-back = 1, 2, 3, and 5 in the emotional and neutral blocks during the eWM task in the scanner at pre-training. Error bars indicate SE. B, The graph reports emotionality ratings across ER task conditions at pre-training. Emotionality (experienced distress) while viewing the film clips was rated on a Likert scale ranging from 1 (extremely positive) to 10 (extremely negative), with 5 (neutral). The conditions were as follows: Neutral, neutral film clips were presented with the instruction to attend to the films without effortful ER; Attend, aversive film clips were presented with the instruction to attend to the films without effortful ER; Regulate, aversive film clips were presented with the instruction to downregulate negative emotions elicited by the films. Error bars indicate SEM.

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    Figure 3.

    A, The graphs represent the eWM training (top graph) and placebo training (bottom graph) groups' performance on their respective tasks across training days. For the eWM training, the graph reports average level of n-back achieved across 20 blocks per day; and for the placebo training, a composite score (including raw score, number of attempts, and reaction time) on the feature match task is reported. Error bars indicate SD. B, The behavioral gains in eWM across training plotted as mean peak level of n-back achieved. A mixed-model ANOVA with time (pre-training and post-training) as the within-subjects factor and training (placebo, eWM) as the between-subjects factor yielded a significant interaction, which showed that the augmentation of eWM observed in the eWM training group was significantly greater than the change in the placebo training group (F(1,30) = 16.61, p < 0.001, longer dotted line). Repeated-measures analyses with time (pre-training, post-training) as the within-subjects factor were then conducted in the two groups separately. These revealed that the placebo training did not lead to any significant changes in eWM performance (Δ mean, −0.59; SD, 1.6; p = 0.18). In contrast, eWM training led to a significant pre-training to post-training increase in eWM performance (Δ mean, 1.59; SD, 1.2; p < 0.001, shorter dotted line). Moreover, eWM performance was significantly greater in the eWM training group compared with the placebo training group at post-training (t = −2.79 p = 0.009). ***p < 0.001, two-tailed significance level. Error bars indicate SDs. C, BOLD activation changes during the eWM task from pre-training to post-training conflated across all levels of n-back for the training groups. Significant interactions of training (placebo, eWM) × time (pre-training, post-training) are described in the main text. The absence of behavioral change after placebo training was mirrored by the absence of brain activation changes (left). In contrast, the behavioral gain in eWM after eWM training (right) was associated with decreased neural activation in the (I) left ventrolateral to dorsolateral PFC (Z = 4.10, −42/42/6), (II) bilateral inferior parietal cortex (Z = 4.87, −57/−48/39) and right precuneus (Z = 3.54, 12/−63/36), (III) inferior/middle temporal gyrus (Z = 5.76, 63/−33/−9), (IV) bilateral middle and posterior cingulum (Z = 3.74, −3/−24/33), and (V) left ACC (Z = 2.53, −1/10/25). All regions were significant at the whole brain with significance set at PFDR < 0.05.

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    Figure 4.

    A, The graph reports mean changes (post-training − pre-training) in emotion ratings for each condition; lower change scores indicate reduced negative affect after training in that condition. B, The graph represents the association between pre-training and post-training changes in ER capacity and changes in eWM. The association is negative because the ER measure represents the pre-training to post-training reduction in reported emotional distress, whereas eWM reports increases in maximum level of n-back achieved at the offline post-training assessment. C, The figure shows the differential effects of eWM training compared with placebo training across time for the Regulate versus Attend conditions in the left superior temporal gyrus. The figure is represented at Puncorrected < 0.001. Error bars indicate SEM. D, The graphs depict the effect of eWM training compared with placebo training across time (pre-training, post-training) for the Regulate versus Attend conditions on BOLD activation in the ROI. Error bars indicate SEM.

  • Figure 5.
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    Figure 5.

    A, The figure shows brain areas that showed greater BOLD activation increases (a contrast of post-training − pre-training) in the Regulate relative to the Attend condition for the eWM training group only at the whole-brain level of analysis. The figure was thresholded at Puncorrected < 0.001. For a full list of activation details, see Table 8. B, The histograms depict mean BOLD activation during the ER task at pre-training and post-training in the regions reported in Figure 5A, which showed an interactive effect of time (pre-training, post-training) and condition (Regulate, Attend) in the eWM training group. Error bars indicate SEM.

Tables

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    Table 1.

    eWM training task-demand-related activation at pre-traininga

    Brain regionL/RCluster size (voxels)Maxima of cluster x/y/z (mm)bZ
    Activation increasec
        Superior frontal gyrusR5524/57/033.56
        Middle frontal gyrusL125−30/51/124.68
    R121627/15/514.80
    R121627/09/604.74
        Inferior frontal gyrusL43−39/21/273.67
        Supplementary motor area/middle cingulateL1216−06/18/454.73
        Middle orbitofrontal gyrusR5527/51/−123.66
        Inferior parietal lobeR167142/−36/425.45
        PrecuneusR1671−09/−57/515.10
        Inferior temporal gyrusR6451/−57/−094.33
        Middle posterior insulaR1830/24/−033.16
        Globus pallidusL13−15/00/−033.10
        CaudateL40−12/06/122.96
        CerebellumL266−12/−54/−454.59
    L266−36/−66/−483.90
    R22436/−54/−364.53
    R22433/−63/−513.89
    R1412/−54/−483.58
    Activation decreased
        Medial prefrontal cortex (medial superior frontal gyrus)R75909/57/214.58
    R1309/33/542.92
    R1112/42/422.77
    R1106/45/482.53
        Subgenual prefrontal cortexR75900/42/−184.32
        Rolandic operculumL3856−48/−24/186.11
    R198851/−21/185.47
        Precentral gyrusR4521/−27/633.63
        Superior temporal gyrusR9760/−57/243.35
        Temporoparietal junctionL142−45/−63/243.63
        Middle temporal gyrusR9760/−60/093.87
    R9754/−51/062.87
        Fusiform gyrusR1939/−33/−183.64
        Amygdala/hippocampusL3856−27/−06/−155.86
    R198827/−06/−154.99
        Parahippocampal regionR8812/−39/−063.04
        InsulaL3856−39/−06/−065.85
    R198839/−03/−094.84
        ThalamusL13−12/−24/032.74
        CuneusL17−03/−84/302.66
    R809/−87/362.67
        Lingual gyrusL8−12/−51/−032.62
    R8815/−48/−093.01
        CerebellumL43−30/−81/−363.85
    R2933/−78/−363.20
    R8818/−54/−183.18
    • ↵aRegions that showed differential activation at n-back = 3 compared with n-back = 1 back on the scanner version of the eWM training task at pre-training. Threshold for whole-brain correction at pFDR < 0.05.

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • ↵ct test contrast: Load 3 > Load 1.

    • ↵dt test contrast: Load 3 < Load 1.

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    Table 2.

    Regions showing differential activation across ER task conditions at pre-training: main effect of typea

    Brain regionL/RCluster size (voxels)Maxima of cluster x/y/z (mm)bZDifferential activation
    Superior medial PFCR346/60/303.98Attend and Regulate > Neutral
    Middle temporal poleR2145/18/303.71Attend > Neutral
    Middle temporal gyrusL46−51/−39/−33.59Attend > Neutral
    −54/−27/−63.35Attend > Neutral
    −48/−21/−153.23Attend > Neutral
    Fusiform gyrusL53−30/−66/−64.23Neutral > Attend
    −24/−81/−64.17Neutral > Attend
    R1330/−66/−33.23Neutral > Attend
    CuneusR1219/−93/184.45Attend > Neutral
    VermisL64−3/−60/−364.11Attend > Neutral
    0/−72/−303.59Attend > Neutral
    • ↵aRegions that showed differential activation across conditions (F contrast) at the whole-brain level with significance level thresholded at puncorrected < 0.001. Subsequent univariate analyses revealed the specific conditions that showed a significant difference (reported in the last column).

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • View popup
    Table 3.

    ROIs showing differential activation across ER task conditions at pre-traininga

    Brain regionL/RNeutral, mean (SD)Attend, mean (SD)RegulateAttend > Neutral, p (η2)Regulate > Attend, p (η2)
    Medial PFCL0.16 (0.35)0.27 (0.39)0.29 (0.30)<0.05 (0.17)
    R0.11 (0.30)0.20 (0.25)0.21 (0.26)<0.05 (0.18)
    Lateral PFC (middle frontal)L0.11 (0.27)0.17 (0.29)0.27 (0.30)<0.05 (0.13)
    R0.12 (0.30)0.22 (0.34)0.38 (0.26)<0.01 (0.23)
    OFCL0.03 (0.30)0.11 (0.31)0.14 (0.24)<0.05 (0.14)
    R0.10 (0.32)0.16 (0.36)0.25 (0.31)<0.05 (0.13)
    Inferior parietal cortexL0.18 (0.36)0.25 (0.40)0.38 (0.35)<0.05 (0.15)
    R0.23 (0.32)0.28 (0.35)0.35 (0.31)<0.05 (0.14)
    • ↵aBOLD activation in the a priori specified ROIs across the different ER conditions. None of the other ROIs showed a significant effect of condition.

    • View popup
    Table 4.

    Regions conjointly activated by the eWM and ER tasks at pre-traininga

    Brain regionL/RCluster size (voxels)Maxima of cluster x/y/z (mm)bZ
    Dorsolateral PFCL82−33/45/65.74
    L30−42/12/395.36
    −42/21/335.09
    L5−39/39/184.92
    R11236/45/185.71
    33/36/275.32
    39/33/365.00
    R7530/12/545.62
    Superior frontal gyrus21/15/605.11
    Middle cingulate cortexL90−9/24/334.98
    R6/21/365.37
    Superior frontal medial gyrus3/27/484.73
    Inferior parietalL378−39/−57/457.53
    −42/−48/397.26
    R37151/−39/45>10
    39/−54/427.06
    PrecuneusL91−9/−69/456.41
    −9/−66/486.26
    InsulaL8−33/15/64.82
    Rolandic opercelumR4545/15/65.72
    Insula39/18/−35.23
    • ↵aRegions that emerged as being activated by both the eWM training task (Load 3 vs Load 1) and the ER task (Regulate vs Attend) in a conjunction analysis of the two tasks. Threshold for whole-brain correction was set at pFWE < 0.05.

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • View popup
    Table 5.

    Regions showing a greater activation decrease from pre-training to post-training after eWM training compared with placebo training for n-back = 3 trialsa

    Brain regionL/RCluster size (voxels)Maxima of cluster x/y/z (mm)bZ
    Dorsolateral PFCL10−48/39/183.77
    Superior frontal gyrusR1127/−6/633.40
    Supramarginal gyrusL8−51/−30/333.46
    R3163/−33/424.00
    Middle temporal gyrusL27−51/−63/154.16
    L17−60/−45/03.78
    R5860/−48/03.91
    Middle occipital lobeL29−45/−81/33.87
    R2042/−81/93.77
    • ↵aRegions that showed greater pre-training to post-training BOLD activation decreases at n-back = 3 in the eWM training group compared with the placebo training group. Threshold for whole-brain correction is puncorrected < 0.001.

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • View popup
    Table 6.

    Regions showing activation changes from pre-training to post-training during the eWM task after eWM traininga

    Brain regionL/RClusterCluster size (voxels)Maxima of cluster x/y/z (mm)bZ
    n-back = 3
        Dorsolateral to middle PFCL6182−33/48/33.71
    6−30/54/213.52
    R2168645/12/184.95
    227/48/184.39
        Middle OFCL6−45/51/−33.49
        Inferior parietal cortexL3260−57/−48/394.56
    3−39/−57/453.24
        Middle temporal gyrusR1109560/−30/−95.06
        Inferior temporal gyrusL594−57/−36/−153.85
        Fusiform gyrusL7−42/−54/−183.07
        InsulaL4−36/15/−33.88
    R242/21/34.06
        ThalamusL45569/−9/183.90
        Inferior occipital gyrusL780−48/−69/−93.34
        CerebellumR82136/−57/−453.25
    n-back = 5
        Lateral PFCR212151/27/−34.28
    248/24/93.99
    43648/15/243.54
        Supplementary motor areaR32312/21/603.74
        Middle cingulateL57−6/−24/333.20
        Angular gyrusL1211−54/−57/364.67
    • ↵aRegions that showed pre-training to post-training BOLD activation increases at n-back = 5 in the eWM training group. Threshold for whole-brain correction was set at pFDR < 0.05.

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • View popup
    Table 7.

    ROIs showing a greater activation increase from pre-training to post-training during the eWM task after eWM training compared with placebo training for n-back = 5 trialsa

    Brain regionL/RPlacebo trainingeWM trainingF(1,31)
    5-back pre-training5-back post-training5-back pre-training5-back post-training
    OFCR−0.08 (0.17)−0.11 (0.26)−0.06 (0.26)0.27 (0.25)8.39*
    Lateral PFC (inferior frontal gyrus)R0.08 (0.19)0.00 (0.35)−0.13 (0.24)0.02 (0.24)5.07**
    Inferior parietal cortexR0.16 (0.35)0.33 (0.52)0.00 (0.39)0.30 (0.43)4.91**
    • ↵aBOLD activation for the ROIs, which showed a significantly different pre-training to post-training activation change related to task difficulty in the eWM training group compared with the placebo training group at the level of n-back = 5.

    • ↵*p < 0.01.

    • ↵**p < 0.05.

    • View popup
    Table 8.

    Regions showing a pre-training to post-training greater increase in BOLD activation during Regulate compared with Attend trials for the eWM training groupa

    Brain regionL/RCluster numberCluster size (voxels)Maxima of cluster x/y/z (mm)bZ
    Inferior OFCL1530−42/33/−34.62
    Medial PFCR4259/60/334.18
    Lateral PFCL1530−57/24/34.80
    L715−27/54/274.07
    R220760/24/154.30
    Inferior frontal operculumL1530−57/15/94.50
    R220745/12/214.31
    R220763/15/184.29
    Lateral superior PFCL642−18/9/603.21
    Supplementary motor areaL642−12/15/634.15
    R6429/12/603.69
    Anterior cingulateR1179/42/303.52
    Middle cingulateL5216−6/−21/393.97
    PrecuneusL5216−6/−51/393.66
    Temporoparietal junctionL3162−54/−54/244.30
    R91063/−51/303.90
    Superior temporal gyrusR101263/0/−63.87
    Middle temporal gyrusL3162−66/−42/123.63
    Middle occipital gyrusL8179−30/−78/214.04
    L8179−42/−72/243.65
    CerebellumR28921/−78/−274.46
    12/−75/−304.45
    • ↵aRegions that showed pre-training to post-training BOLD activation increases for the Regulate relative to the Attend condition in the eWM training group at the whole-brain level. Threshold for whole-brain correction is puncorrected < 0.001.

    • ↵bStereotaxic coordinates of peak voxels in MNI space.

    • View popup
    Table 9.

    ROIs showing a pre-training to post-training greater increase in BOLD activation during Regulate compared with Attend trials for the eWM training groupa

    Brain regionL/RAttendRegulateF(1,16)η2
    Pre-trainingPost-trainingPre-trainingPost-training
    Subgenual ACCL−0.03 (0.22)0.06 (0.20)−0.01 (0.21)0.13 (0.26)4.65*0.24
    ACCL0.27 (0.27)0.21 (0.40)0.09 (0.36)0.26 (0.38)5.68*0.28
    OFCL0.14 (0.23)0.12 (0.26)0.04 (0.28)0.23 (0.31)8.21*0.35
    Medial PFCL0.13 (0.16)0.11 (0.22)0.06 (0.19)0.11 (0.24)4.60*0.24
    Lateral PFC (middle frontal gyrus)L0.14 (0.26)0.11 (0.28)0.01 (0.32)0.19 (0.30)7.62*0.34
    R0.21 (0.34)0.16 (0.40)0.06 (0.33)0.23 (0.41)4.85*0.24
    Inferior parietal cortexL0.34 (0.19)0.29 (0.26)0.21 (0.24)0.34 (0.28)5.23*0.26
    • ↵aSignificant ROIs for the same contrast.

    • ↵*p < 0.05.

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Training the Emotional Brain: Improving Affective Control through Emotional Working Memory Training
Susanne Schweizer, Jessica Grahn, Adam Hampshire, Dean Mobbs, Tim Dalgleish
Journal of Neuroscience 20 March 2013, 33 (12) 5301-5311; DOI: 10.1523/JNEUROSCI.2593-12.2013

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Training the Emotional Brain: Improving Affective Control through Emotional Working Memory Training
Susanne Schweizer, Jessica Grahn, Adam Hampshire, Dean Mobbs, Tim Dalgleish
Journal of Neuroscience 20 March 2013, 33 (12) 5301-5311; DOI: 10.1523/JNEUROSCI.2593-12.2013
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