آمیگدال فعال و حالات صورت: تبعیض احساسات عیان در مقابل پردازش احساسات ضمنی

Abstract Emotion recognition is essential for social interaction and communication and is a capacity in which the amygdala plays a central role. So far, neuroimaging results have been inconsistent as to whether the amygdala is more active during explicit or incidental facial emotion processing. In consideration of its functionality in fast automatic evaluation of stimuli and involvement in higher-order conscious processing, we hypothesize a similar response to the emotional faces presented regardless of attentional focus. Using high field functional magnetic resonance imaging (fMRI) specifically optimized for ventral brain regions we show strong and robust amygdala activation for explicit and implicit processing of emotional facial expressions in 29 healthy subjects. Bilateral amygdala activation was, however, significantly greater when subjects were asked to recognize the emotion (explicit condition) than when required to discern the age (implicit condition). A significant correlation between amygdala activation and emotion recognition, but not age discrimination performance, emphasizes the amygdala's enhanced role during conscious emotion processing.

1. Introduction The ability to correctly recognize emotions in facial expressions plays an essential role in social communication and, evolutionarily, is important for survival (Darwin, 1872). The neural basis of facial emotion processing includes a network of cortical and subcortical structures, centering on the amygdala (Adolphs, 2002; Adolphs, Gosselin et al., 2005; LeDoux, 1995; Morris, Öhman, & Dolan, 1999). Growing evidence supports the notion that the amygdala is essential for several domains of emotional behavior, such as fear conditioning (Blair, Sotres-Bayon, Moita, & LeDoux, 2005), emotional memory (Adolphs, Tranel, & Buchanan, 2005), mood induction (Habel, Klein, Kellermann, Shah, & Schneider, 2005) and emotion discrimination (Gur, Schroeder et al., 2002). Amygdala dysfunction has been investigated in brain lesion (Adolphs et al., 2005a and Adolphs et al., 2005b) and psychiatric patients (Kohler et al., 2003 and Surguladze et al., 2004; Townshend & Duka, 2003). The amygdala's functionality in the early phases of processing is suggested by rich cortical afferents from sensory cortices and fast input routes via the thalamus, as well as extensive output routes to prefrontal and other cortical and subcortical areas. The amygdala's input provides both highly processed and raw information sufficient to prompt fast automatic responses. Accordingly, the amygdala has been considered “the gateway to the emotions” (Aggleton & Mishkin, 1986). Its role has been implicated in evaluating whether a stimulus is pleasant or unpleasant, harmless or dangerous, with a focus on facial expressions of emotions as particularly relevant sources of information (see Hariri, Tessitore, Mattay, Fera, & Weinberger, 2002). Given this functionality, the amygdala should be responsive to all facial expressions of emotion, regardless of whether or not attention is directed toward emotional aspects. This hypothesis has elicited only limited testing with neuroimaging tools and with quite contradictory results. Several studies reported stronger activation of the amygdala-hippocampal area during unattended emotion processing, that is, implicit or passive (gender or age discrimination), compared to explicit tasks (emotion recognition or positive/negative discrimination), in which the depicted emotion was the focus of attention (Critchley et al., 2000; Hariri, Bookheimer, & Mazziotta, 2000; Keightley et al., 2003 and Lange et al., 2003). The opposite, however, has also been found: no activation during implicit processing of disgusted faces (Gorno-Tempini et al., 2001) or less activation during incidental emotional processing compared to explicit emotion recognition (Gur, Schroeder et al., 2002). Winston, O’Doherty, and Dolan (2003) presented two faces at a time and asked subjects to either identify the more emotional (explicit condition) or more male face (implicit condition). Task independent amygdala responses were found when high- and low-intensity expressions were compared across four emotions. This study did not, however, require subjects to actually perform emotion identification. Furthermore, an interaction between valence and attention has also been reported (Williams, McGlone, Abbott, & Mattingley, 2005), with stronger activation to unattended, potentially threatening facial stimuli, in contrast to attended stimuli, whilst responses to happy faces were greater when attended. Some of this divergence may be attributed to methodological issues. Most studies applied low-resolution measurement methods, which exacerbate susceptibility-related signal dropout (Merboldt, Fransson, Bruhn, & Frahm, 2001)—particularly affecting the amygdala. Furthermore, most studies used a block presentation design, which is particularly vulnerable to habituation (i.e. Büchel, Dolan, Armony, & Friston, 1999) and movement artifacts (Robinson & Moser, 2004). The choice of analysis approaches may also affect results given the small signal changes in fMRI. Finally, implicit tasks of gender or age discrimination with a binary division of stimuli (male/female and younger/older than 30) and positive/negative decisions are usually much simpler than tasks assessing emotion recognition ability, and task complexity might disengage emotion processing. The present study was designed to address these issues. We used a high-resolution data acquisition (Echo-Planar-Imaging, EPI) protocol specifically developed for imaging the amygdala region at 3 T, to reliably detect BOLD (blood-oxygen-level-dependent) based activation changes (Robinson, Windischberger, Rauscher, & Moser, 2004; Robinson et al., 2005). In particular spatial resolution, slice orientation and echo time were optimized for the high field strength and ventral brain region, giving measurements that yield 60 percent higher time-series signal-to-noise ratio (SNR) in the amygdala than measurements with standard EPI parameters. The effects of physiological artifacts have been compensated for in post-processing, increasing sensitivity. An event-related presentation design was used, which is more flexible and more robust against scanner drifts and head motion. The stimulus material has been pre-validated, and the implicit task has been re-designed to be more demanding and engaging. Whole-brain analysis has been supplemented by ROI approaches. With these methodological improvements we attempted to examine the extent to which the attentional focus of the task – implicit or explicit emotional processing – influences neural activation in the amygdala.

3. Results 3.1. Behavioral performance Emotion recognition accuracy was 90.3 percent (±5.9, mean ± SD) on average for male and 90.6 percent (±5.8) for female subjects. The mean percent correct for age discrimination was 39.1 percent (±10.1) and 45.1 (±9.8), respectively. Reaction time for emotion recognition was 2.5 s (±0.3) in males and 2.3 s (±0.4) in females, for age discrimination 2.5 s (±0.3) and 2.6 s (±0.3), respectively. Levene tests for homogeneity of variances established homoscedasticity for emotion recognition (p = 0.94) and age discrimination (p = 0.90) performance. Shapiro–Wilk tests demonstrated a normal distribution for both variables (emotion p = 0.16; age p = 0.11). The two-way ANOVA with gender as between-subject factor and task as within-subject factor revealed only a significant task difference (F(1,23) = 618.9, p = 0.0001) without any gender differences (F(1,23) = 1.40; p = 0.25). In the equivalent ANOVA for reaction time (Levene tests: emotion recognition (p = 0.68) and age discrimination (p = 0.83); Shapiro–Wilks (emotion p = 0.57; age p = 0.99)) similarly a main effect for task emerged (F(1,23) = 5.74, p = 0.03) as well as a significant task-by-gender interaction (F(1,23) = 7.85, p = 0.01), reflecting relatively faster response times for women on emotion compared to age identification. However, post hoc tests decomposing this interaction remained not significant. For age discrimination reaction time was not significantly different between males and females (t(23) = −1.11, p = 0.28) as was reaction time for emotion discrimination (t(23) = 1.83, p = 0.08). 3.2. Functional data 3.2.1. Whole brain analyses This study was specifically designed to clarify the role of the amygdala in recognizing and processing basic emotions, investigating the influence of task instruction on its activation. As hypothesized, significant BOLD signal increases were found in the amygdala bilaterally, during explicit and implicit processing of emotional faces (Fig. 2 and Fig. 3). There was also activation in adjacent areas: the hippocampus, fusiform gyrus, temporal pole and brainstem. Differences between tasks were tested by paired t-tests (explicit–implicit and implicit–explicit). Results revealed significant differences showing stronger left amygdala activation during explicit emotion recognition, as presented in Fig. 3. A higher degree of fusiform, brainstem and temporal activation also emerged during emotion discrimination, pointing to emotion-specific functions of these areas during conscious processing. See Table 1 summarizing main activated brain regions for explicit and implicit face processing separately as well as for direct comparison. Group results overlaid on mean echo-planar images revealing bilateral amygdala ... Fig. 2. Group results overlaid on mean echo-planar images revealing bilateral amygdala activation (p = 0.05, FWE corrected) as well as temporal and fusiform gyrus, cerebellum and brainstem involvement for explicit emotion processing (emotion recognition, a), implicit emotion processing (age discrimination, b) and the difference between explicit and implicit emotion processing (c). Figure options Group activation results for explicit (left) and implicit (right) emotion ... Fig. 3. Group activation results for explicit (left) and implicit (right) emotion processing overlaid on a surface rendered brain showing strong bilateral amygdala activation during both conditions. Figure options To exclude the possibility that findings resulted from an unequal number of stimuli in each condition, we performed an additional analysis pooling randomly 12 emotion task stimuli. Although the effect was somewhat attenuated and significant only at a level of p = 0.001 uncorrected, the contrast of 12 emotion stimuli against the 12 age stimuli revealed nearly identical results: explicit emotional processing produced a stronger amygdala response than implicit processing of such stimuli during the age identification task. 3.2.2. ROI analyses The three-way repeated measures analysis of variance (Fig. 4) with gender as between-subject factor and condition (explicit, implicit) and laterality (left, right) as within-subject factors revealed a significant main effect for condition (F(1, 27) = 20.63; p = 0.0001) without any further significant main effects or interactions. Hence the ROI analysis confirmed the whole brain result that the amygdala response is significantly enhanced during explicit processing. ROI results for the amygdala. Mean parameter estimates (±SEM) extracted from the ... Fig. 4. ROI results for the amygdala. Mean parameter estimates (±SEM) extracted from the amygdala ROI for male and female subjects, and left and right amygdala regions. Only a main effect of condition emerged, pointing to higher responsivity of the amygdala during explicit emotion processing, an effect which is similar in both genders and for both amygdalae. Figure options Fig. 5 shows the mean activation differences in the amygdala between the explicit and implicit emotion processing task, for each subject. Of the 29 participants 26 demonstrated reduced amygdala response during age compared to emotion discrimination. Scatterplot of individual differences of mean parameter estimates in the ... Fig. 5. Scatterplot of individual differences of mean parameter estimates in the amygdala ROIs between explicit and implicit emotion processing for male and female subjects indicating the stronger response during the explicit condition in most of the subjects. Figure options To control for the different number of stimuli and in correspondance to the whole brain analysis, an ROI analysis (ANOVA) using only 12 emotion and 12 age stimuli was also performed and confirmed main analysis results (condition: F(1, 27) = 7.24, p = 0.01), see Table 2. Table 2. Region of interest analysis for the amygdala Amygdala parameter estimates Left p-Value Right p-Value Emotion recognition 2.92 ± 0.42 <0.0001 2.59 ± 0.37 <0.0001 Age discrimination 2.16 ± 0.48 <0.0001 2.05 ± 0.43 <0.0001 Parameter estimates (±SEM) of activation during both tasks, separately for left and right amygdala ROI (12 emotion vs. 12 age stimuli). Values have been tested on their significance applying one-sample t-tests. No significant differences between left and right amygdala were obtained for emotion recognition, nor age discrimination. Table options A significant correlation between activation levels in the voxel with highest activation (located in the right amygdala as shown by SPM random effects analysis) and behavioral performance during emotion recognition (r = 0.42, p = 0.04, see Fig. 6 left) further supports the role of the amygdala in conscious emotional processing. No corresponding correlation was observed for age discrimination (right: r = 0.19, p = 0.36, see Fig. 6 right). Correlations for the left amygdala, however, remained not significant (emotion recognition r = 0.29, p = 0.16, age discrimination r = 0.21, p = 0.31). Scatterplot of correlation analysis between voxel with highest activation taken ... Fig. 6. Scatterplot of correlation analysis between voxel with highest activation taken from SPM random effects analysis and performance for explicit emotion recognition (left) and implicit emotion processing (right) across all subjects indicating a significant positive correlation between emotion recognition accuracy and amygdala response only.