Individual differences in socioaffective skills influence the neural bases of fear processing: the case of alexithymia

Abstract

Being exposed to fear signals makes us feel threatened and prompts us to prepare an adaptive response. In our previous studies, we suggested that amygdala (AMG) and premotor cortex (PM) play a role in the preparation of the observers' motor response required by the situation. The present experiment aimed at assessing how interindividual differences in alexithymia--a personality trait associated with deficits in emotional reactivity and regulation--influence the neural network associated with the perception of fear. Using fMRI, we scanned 34 healthy subjects while they were passively observing fearful body expressions. Applying a dimensional approach, we performed correlation analyses between fear-related brain areas and alexithymia scores among all participants. Using a categorical approach, we conducted a between-group comparison (13 high vs. 12 low-alexithymia subjects). Our results were threefold. First, the right AMG activity in response to fearful stimuli was negatively correlated with the level of difficulty to identify emotions. Second, PM activity was linked to reduced subjective emotional reactivity. Third, the between-group comparison revealed greater activity in anterior cingulate cortex (ACC) for high than low-alexithymia scorers. Moreover, the relationship between ACC and PM was in opposite direction in individuals with high (negative link) and low (positive link) alexithymia. Therefore, compared to our previous findings, we hereby further reveal how ACC interacts with PM to sustain self-regulation of one's own emotional state in response to threatening social signals. Moreover, this neural mechanism could account for the description of the "cold-blooded" personality of individuals with alexithymia.

Figure 1

Alexithymia‐related activations during emotional tasks. The activations' peak of 14 studies revealed during either direct comparison between alexithymic and non‐alexithymic groups or correlation analyses with alexithymia scores (BVAQ‐B or TAS‐20) was superimposed on sagittal sections of the MNI brain, one for the medial frontal cortex (x = 0, anterior cingulate cortex and superior medial frontal gyrus) and one for the amygdala (x = 20); (1) [Berthoz et al., 2002a]; (2) [Huber et al., 2002]; (3) [Kano et al., 2003]; (4) [Leweke et al., 2004]; (5) [Mantani et al., 2005]; (6) [Mériau et al., 2006]; (7) [Li and Sinha, 2006]; (8) [Kano et al., 2007]; (9) [Moriguchi et al., 2007]; (10) [Frewen et al., 2008]; (11) [Kugel et al., 2008]; (12) [Silani et al., 2008]; (13) [Reker et al., 2009]; (14) this study; PTSD, posttraumatic stress disorder; *used ROI approach, and therefore coordinates were not available.

Figure 2

Correlations between activity in key regions of the fear network and alexithymia scores. A: The right amygdala (AMG): A1—Group average activation of amygdala superimposed on a coronal section of the MNI brain. A2—Negative correlation between AMG activity and BVAQ‐B B3 scores, which measure subjects' difficulties in identifying emotions. B: The right premotor cortex (PM): B1—Group average activation of the PM superimposed on a sagittal section of the MNI brain. B2—Negative correlation between PM activity and BVAQ‐B B4 scores that measure low emotional reactivity. C: The right anterior cingulate cortex (ACC): C1—Group average activation of ACC revealed by the comparison between HA and LA groups, superimposed on a sagittal section of the MNI brain. C2—Positive correlation between ACC activity and BVAQ‐B B4 scores that measure low emotional reactivity. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

Correlations between three key brain areas (ACC, PM, and AMG) in high and low‐alexithymia scorers. Correlation analyses between AMG (top) and PM (bottom) activities and ACC activity in subjects with high alexithymia (in red) and low alexithymia (in blue). The dots correspond to subjects' mean contrast values in a 10‐mm ROI (AMG and PM) for the contrast Fear versus Neutral relative to the mean contrast values in the ACC ROI extracted from the same contrast. Note that the slopes between ACC and PM are significantly different between the two groups and in opposite direction (HA: r = −0.525; LA: r = 0.419), whereas the slopes between ACC and AMG did not differ between the two groups.