مکانیسم های فیزیولوژی عصبی در مدولاسیون عاطفی توجه: فعل و انفعال بین حساسیت تهدید و کنترل توجه

Abstract Processing task-irrelevant emotional information may compromise attention performance, particularly among those showing elevated threat sensitivity. If threat-sensitive individuals are able to recruit attentional control to inhibit emotional processing, however, they may show few decrements in attention performance. To examine this hypothesis, attention performance was measured in three domains—alerting, orienting, and executive attention. Task-irrelevant fearful, sad, and happy faces were presented for 50 ms before each trial of the attention task to create a mildly competitive emotional context. Electroencephalographic recordings were made from 64 scalp electrodes to generate event-related potentials (ERPs) to the faces. Participants reporting high threat sensitivity showed enhanced ERPs thought to reflect emotional processing (P200) and attentional control (P100 and N200). Enhanced N200 following fearful faces was linked to sustained and even slightly improved executive attention performance (reduced conflict interference) among high threat-sensitive individuals, but with decrements in executive attention among low threat-sensitive individuals. Results are discussed in terms of cognitive processing efficiency and the balance between threat sensitivity and attentional control in relation to executive attention performance. Results may have implications for understanding automatic and voluntary attentional biases related to anxiety.

Results 2.1. Descriptive statistics Table 1 presents ERP amplitudes and attention scores for correct trials only. Within each domain of attention, efficiency scores following each face type were highly inter-correlated (r = .69–.71). Because there were no gender-related hypotheses and no gender differences in study variables emerged, gender was not included in analyses reported below. Table 1. Descriptive statistics for ERP amplitudes and attention performance scores Region Emotion Fear M (S.D.) Sad M (S.D.) Happy M (S.D.) Total M (S.D.) P100 Right 5.15 (2.84) 5.10 (3.11) 5.14 (3.21) 5.13 (2.94) Left 4.44 (2.74) 4.89 (2.78) 4.56 (2.62) 4.63 (2.62) Midline 2.39 (2.20) 2.41 (2.57) 2.27 (2.37) 2.36 (2.26) N140 Right −5.89 (4.30) −5.44 (4.04) −5.60 (4.24) −5.64 (4.10) Left −4.89 (3.57) −4.67 (3.50) −4.64 (3.53) −4.74 (3.42) Midline −3.66 (2.95) −3.39 (3.13) −3.56 (2.86) −3.54 (2.86) P200 Right 6.90 (4.16) 6.97 (3.89) 6.69 (3.82) 6.85 (3.85) Left 5.94 (3.53) 6.25 (3.35) 6.09 (2.95) 6.10 (3.18) Midline 5.25 (2.73) 5.24 (2.48) 5.14 (2.34) 5.21 (2.34) N200 Right −3.37 (1.80) −3.39 (1.78) −3.24 (1.61) −3.33 (1.64) Left −2.89 (1.77) −2.64 (1.64) −2.86 (1.59) −2.78 (1.54) Midline −3.06 (2.00) −3.05 (2.02) −2.84 (1.64) −2.98 (1.78) Alerting 25.06 (28.98) 33.72 (35.41) 26.67 (34.87) 28.48 (21.53) Orienting 42.07 (33.84) 43.50 (31.00) 43.28 (35.96) 42.95 (25.00) Executive attention 101.00 (46.81) 88.49 (47.63) 102.01 (47.84) 97.16 (42.37) Error rates (%) 3 (4) 4 (4) 3 (3) 3 (4) Table options 2.2. Emotional faces and arousal At the completion of the attention task, participants rated each face using the Self-Assessment Mannequin technique (Lang et al., 1998). Faces were rated on a 1–5 scale for arousal, with 5 indicating highly arousing, and a 1–5 scale for valence, with 1 being very positive and 5 being very negative. Although there were high levels of inter-correlation among emotions for arousal and valence ratings (r = .54–.88), sad faces were rated as less arousing than fearful, t(35) = −4.64, p < .001, and happy faces, t(35) = −3.08, p < .01 (sad M = 1.32, S.D. = 0.81; fearful M = 1.63, S.D. = 0.89; happy M = 1.78, S.D. = 0.99). Happy faces were rated as more positive than fearful, t(35) = −7.82, p < .001, and sad faces, t(35) = −9.10, p < .001, and fearful faces more positive than sad faces, t(35) = −6.04, p < .001 (sad M = 3.56, S.D. = 0.59; fearful M = 3.19, S.D. = 0.51; happy M = 2.04, S.D. = 0.56). Thus, overall, sad faces were perceived as less arousing but more negative than fearful and happy faces. To confirm the characterization of ERP components related to emotional processing, it was examined whether links between BIS sensitivity and arousal ratings for faces depended on ERP responses, particularly N140 and P200. That is, it was predicted that faces would be perceived as arousing mainly when greater emotional processing resources were recruited after viewing them. To test this, a series of hierarchical regressions were conducted in which the dependent variable was subjective ratings of arousal when viewing fearful, sad, and happy faces. P100, N140, P200, and N200 amplitudes at maximal electrode regions were entered in the first step, BIS was entered in the second step, and the interactions between BIS and ERP amplitudes were entered in the third step. If the interaction term's contribution to r2 was significant (p < .05), moderation effects were plotted using simple regression equations ( Lang et al., 1998). These recast the significant interactions as the regression of one criterion on one predictor ( Aiken and West, 1991 and Finney et al., 1984). The criterion on the y-axis was plotted against two levels of the predictor (BIS), 1 S.D. below the mean (low) and 1 S.D. above the mean (high). Plotted regression lines represent two levels of the moderator (high and low ERP amplitudes also one standard deviation below and above the mean). Predictor variables were centered to reduce problems of lack of invariance of regression coefficients and multicollinearity ( Aiken and West, 1991). Table 2 lists regression coefficients with all variables entered. As BIS sensitivity increased, arousal increased but only when P200 amplitudes were relatively low. The low BIS group reported predicted increases in arousal to faces when P200 amplitudes to faces were relatively high ( Fig. 4). Regressions with other ERPs did not reach significance. Table 2. Regressions: effects of BIS and ERP amplitudes on arousal and executive attention Steps and predictors F B B R ΔF Arousal Step 1. P200—fear faces <1 .03 .13 .00 <1 Step 2. BIS <1 −.07 −.04 .01 <1 Step 3. P200 × BIS −2.17* −.18 −.41 .14 4.72* Step 1. P200—sad faces <1 −.004 −.02 .04 1.22 Step 2. BIS <1 −.12 −.07 .04 <1 Step 3. P200 × BIS −2.00* −.16 −.37 .14 4.01* Executive attention Step 1. N200—fear faces <1 −.01 −.02 .01 <1 Step 2. BIS <1 .07 .05 .01 <1 Step 3. N200 × BIS −2.12* −.24 −.37 .13 4.49* *p < .05. Coefficients are those generated when all steps are entered. Table options The association between BIS and arousal varied depending on the amplitude of ... Fig. 4. The association between BIS and arousal varied depending on the amplitude of P200 following fearful and sad faces. Figure options 2.3. Links between BIS and ERP measures of emotional and attentional processing Next, it was tested whether increased BIS sensitivity was related to enhanced ERP responses related to emotional processing and the recruitment of cognitive control. Consistent with this, correlational analyses (see Table 3) showed that BIS sensitivity was positively correlated with P100, P200, and N200 amplitudes, indicating that as BIS sensitivity increased, ERP responses increased. This question was further examined by conducting four 2 (BIS: low versus high) × 3 (Emotion: fear, sad, happy) × 3 (Electrode Region: right, midline, left) repeated-measure ANOVAs, one for each component. Dependent variables were peak amplitudes at right, left, and midline (a) posterior electrode regions for components P100, N140, and P200; and (b) anterior electrode regions for N200. Greenhouse–Geisser corrections were inspected but did not differ from uncorrected values. Significant effects were followed with LSD tests or paired t-test. Table 3. Correlations between ERPs and study variables BIS Arousal Valence Alerting Orienting Conflict Fear P100 .38* −.09 .10 .09 −.12 .20 N140 −.02 −.12 −.17 .01 −.03 −.16 P200 .42* −.05 −.26 .19 −.10 −.01 N200 .46** −.20 −.19 .17 −.20 .13 Sad P100 .38* −.10 .30 −.01 .18 .28 N140 .02 −.15 −.13 −.21 .23 −.21 P200 .35* −.19 −.02 −.01 .17 .07 N200 .33* −.25 .04 −.11 .09 .15 Happy P100 .39* −.13 .01 −.10 .13 .08 N140 .05 −.41* −.02 −.11 −.02 −.11 P200 .38* −.09 .22 .06 .19 .06 N200 .29 −.24 .28 −.03 .17 −.01 Note. ERPs were absolute values to aid interpretation of findings. To reduce the number of correlations, right hemisphere electrode values were used. Amplitudes were maximal in the right lateralized scalp regions, although patterns of correlations were similar across all electrode regions. *p < .05; **p < .01. Table options P100 and P200 amplitudes were maximal at right and left lateralized compared to central sites, and N140 and N200 amplitudes were maximal at right compared to left and central sites, all t-test p < .001 for P100 and N140, p < .01 for P200, and p < .05 for N200. The effect of electrode region was not moderated by face type or BIS. As seen in Fig. 5, main effects of BIS were consistent with correlational analyses, showing that ERPs reflecting emotional processing (P200) and attentional inhibition (P100 and N200) were enhanced in the high versus low BIS group for all face types. For P100, (F(1,34) = 12.53, p < .001, partial η2 = .27; M = 5.33, S.D. = 2.37 versus M = 3.01, S.D. = 1.54, t(34) = −3.54, p < .001); for P200, (F(1,34) = 7.77, p < .01, partial η2 = .19; M = 7.39, S.D. = 3.10 versus M = 4.98, S.D. = 2.08, t(34) = −2.79, p < .01); and for N200, (F(1,34) = 6.70, p < .01, partial η2 = .17; M = −3.74, S.D. = 1.67 versus M = −2.47, S.D. = 1.28, t(34) = −2.59, p < .05). Effects did not reach significance for N140 amplitudes, and counter to prediction effects were not greater for fearful versus sad or happy faces. Grand-averaged ERP responses for high (solid line) vs. low (dashed line) BIS ... Fig. 5. Grand-averaged ERP responses for high (solid line) vs. low (dashed line) BIS groups across all emotions for the P100 and P200 components (right posterior electrode PO8; top panel) and for N200 (right anterior electrode FC4; bottom panel). The amplitudes of these components were most pronounced in the high vs. low BIS group. Figure options 2.4. Attention performance: behavioral data Before examining links between ERP responses and attention performance, it was of interest to test whether emotional factors alone influenced attention performance. Three 2 (low versus high BIS) × 3 (Emotion: fear, sad, happy) repeated measure ANOVAs were conducted to examine the effects of BIS and face type on attention performance (alerting, orienting, and executive attention separately). Multivariate effects did not reach significance. Within-subjects contrast for executive attention, however, showed a main effect of Emotion, F(1, 34) = 5, 23, p < .05: executive attention was improved (conflict interference reduced) following sad versus fearful, t(35) = 2.02, p < .05, and sad versus happy faces, t(35) = 2.02, p < .05. 2.5. Attention performance: effects of BIS and ERPs Results thus far suggest that increased BIS sensitivity was linked to enhanced emotional processing and recruitment of cognitive control after viewing task-irrelevant emotional faces. The goal of the next set of analyses was to examine whether enhanced N200 will reduce the negative impact of threat-related fearful faces on executive attention among those showing high threat sensitivity, but in low threat-sensitive individuals interfere with attention performance. As seen in Table 3, ERPs alone were not correlated with attention performance. In a series of hierarchical multiple regressions, the dependent variables were alerting, orienting, and executive attention (conflict) scores following presentation of fearful, sad, and happy faces. P100, N140, P200, and N200 amplitudes at maximal electrode regions were entered in the first step, BIS was entered in the second step, and the interactions between BIS and ERP amplitudes were entered in the third step. If the interaction term's contribution to R2 was significant (p < .05), moderation effects were plotted using simple regression equations ( Lang et al., 1998). The criterion on the y-axis was plotted against two levels of the predictor (BIS), 1 S.D. below the mean (low) and 1 S.D. above the mean (high). Plotted regression lines represent two levels of the moderator (high and low ERP amplitudes 1 S.D. below and above the mean). Table 2 lists regression coefficients with all variables entered. Analyses for alerting and orienting did not reach significance. Although behavioral effects suggested that executive attention was improved following sad faces, analyses with ERPs did not. Instead, as predicted, enhanced N200 reduced the negative impact of fearful faces on executive attention performance, but this depended on level of threat sensitivity: as BIS sensitivity increased, executive attention improved (conflict decreased) but only for those showing relatively high N200 to fearful faces (see Fig. 6). Low BIS combined with enhanced N200 was linked to the lowest executive attention scores. No other significant effects emerged. The association between BIS and executive attention performance varied depending ... Fig. 6. The association between BIS and executive attention performance varied depending on the amplitude of N200 following fearful faces.