Means including standard error bars of the parameter estimates extracted for the lateralized functional regions-of-interest. Graph illustrates enhanced BOLD activation for the emotional as compared to the neutral gestures, most pronounced for the middle finger category and generally more prominent in the right hemisphere.
In the left hemispheric fROI, results confirmed the main effect of picture category (F(2, 58) = 17.83, p < .001; see Fig. 2.5, left). Testing all gesture categories against each other by means of post-hoc comparisons yielded highly significant activation increases for both emotional categories compared to the neutral pointing finger gesture (thumb vs. index: F(1, 29) = 8.92, p < .01; middle vs. index: F(1, 29) = 30.89, p < .001). Also, this effect was stronger for the unpleasant as compared to the pleasant category (middle vs. thumb: F(1, 29) = 10.42; p < .01).
Calculation of the same analyses for the right lateralized fROI also resulted in a highly significant main effect for picture category (F(2, 58) = 40.9, p < .001; see Fig. 2.5, right). On the right side however, there was just a trend indicating increased BOLD-activation when comparing the pleasant thumb-up with the neutral index finger gesture (F(1, 29) = 3.81, p = .06). In contrast, the unpleasant picture category differed significantly from both the neutral (F(1, 29) = 56.04, p < .001), as well as the pleasant gesture (F(1, 29) = 42.82, p < .001).
Discussion
Brain imaging studies examining the neural processing of emotionally meaningful stimuli have consistently demonstrated enhanced BOLD activity in extra-striate visual cortex, as well as limbic and para-limbic structures when comparing emotional and neutral materials. The utilized stimuli in these studies include both naturalistic scenes with no specific social quality, as well as stimuli representing non-verbal communicative signals of high social relevance, such as emotional facial expressions or body language. Together, these emotional stimuli are characterized by high evolutionary significance. Extending this research, the present study examined for the first time to what degree the emotional meaning eliciting those effects is a function of phylogenetic preparedness or whether it might also get attached to stimuli by social learning. For this purpose, a new class of socially relevant stimuli was assessed whose motivational significance is highly symbolic and depends on a shared cultural background. This was realized by utilizing simple emblematic hand-gestures bearing a clear semantic, yet highly symbolic meaning unequivocally understood by the examined subject group. In terms of perceived emotionality, these gestures included one pleasant and one unpleasant, as well as one neutral category.
Consistent with a priori expectations, enhanced neural processing was found in extrastriate cortical areas while viewing the emotionally unpleasant middle-finger jerk gesture as compared to the other picture categories. This was confirmed both by conservative 2nd-level random-effects testing, as well as a more detailed and statistically less constrained region-of-interest analysis. Consistent with these observed differences in brain activity, subjects exclusively rated the middle finger gesture as higher arousing than the others which did not differ from each other in terms of perceived arousal (see Fig. 1.3). This is in line with reports from earlier studies showing that the brain’s processing of emotional picture materials covaries strongly with the arousal dimension whereas valence has almost no predictive value regarding processing differences in associative visual cortex (Bradley et al., 2003; Junghöfer et al., 2005). However, even though the observed processing differences showed the strongest effect for the relatively higher arousing middle-finger category, very liberal explorative inspection of differences between the emotionally pleasant thumb up and the neutral index finger gesture revealed similar patterns of enhanced brain activity (see Fig. 1.4). Taken together, these results demonstrate the preferential processing of
emotionally salient meaningful hand gestures in associative visual cortical areas.
These observations are consistent with former studies showing enhanced BOLD activity in corresponding areas during the perception of emotionally arousing naturalistic scenes, as well as emotional facial expressions and body posture (e.g., Bradley et al., 2003; Breiter et al., 1996; de Gelder et al., 2004; Hadjikhani & de Gelder, 2003; Junghöfer et al., 2005; Junghöfer et al., 2006; Pessoa et al., 2002a;
Sabatinelli et al., 2004; Sabatinelli et al., 2005; Vuilleumier et al., 2001).
The observation that the relatively highest degree of brain activity was found for the insulting gesture may not only be accounted for by considering the gestures’
respective arousal level. This result also relates to studies examining facial affect which report maximal modulation for angry faces, also signaling potential threat (Pourtois et al., 2006; Schupp et al., 2004c). Moreover, several studies utilizing psychophysical measures demonstrated that anger was the emotion most reliably decoded from stimuli depicting dance or gesture (Boone & Cunningham, 1998;
Dittrich et al., 1996; Pollick et al., 2001; Pollick et al., 2002). Finally, studies examining emotional body language consistently report maximal neuronal activation in response to fearful body postures (de Gelder et al., 2004; Hadjikhani & de Gelder, 2003). Therefore, existing evidence suggests that detecting angry or threatening non-verbal signals sent by interaction partners may be of special significance.
Adapting an evolutionary perspective, some authors suggest that threatening facial expressions are prototypical cues to activate the human fear system (Lang et al., 2000; Öhman, 1986; Öhman & Mineka, 2001). However, considered from a two-dimensional model of emotion (Cacioppo et al., 1999; Lang et al., 1997) in which the arousal dimension is proposed to reflect the respective activation level of one of two affective sub-systems – one subserving appetitive, the other aversive affects – emotionally enhanced physiological reactions are not restricted to evolutionarily important cues but are rather a consequence of the increased activation of either motivational sub-system. The present results are perfectly in line with this account, showing a close correspondence between the subjective arousal ratings and measured neural activation. Therefore, whereas the experimental stimuli’s respective arousal can be viewed as confound with respect to the specific relevance of fear-related stimuli, it might rather be considered as reflecting the engagement of the underlying defensive
motivational system. The present findings are in perfect correspondence to these assumptions.
Additional areas of enhanced brain activity were found specifically contrasting the middle finger gesture with the other categories. These additional activations included regions of both the medial, as well as the lateral parietal cortex. In the former case, this included specifically the precuneus, whereas in the latter case areas in the Superior and Inferior parietal lobules and most prominently in the postcentral gyrus at the vicinity to the supramarginal gyrus showed increased functional activity. The overall extension of these postcentral activation clusters from dorsal to ventral encompassed roughly the somatotopic areas of the hand and the fingers. This is in line with reports from earlier imaging studies highlighting a special involvement of the parietal cortex during the observation of hand movements, including grasping (Bonda et al., 1996; Grafton et al., 1992), pantomimes of tool use (Moll et al., 2000) or even movements without any meaning (Decety et al., 1997;
Grezes et al., 1998). Using a picture matching paradigm, Hermsdörfer and colleagues (2001) showed subjects static pictures of various meaningless gestures being defined either by whole hand postures (“hand gestures”) or by specific finger-related anatomic configurations (“finger gestures”). The found pattern of BOLD activity elicited by finger gestures closely resembles the results of the present study. Activations in parieto- and temporo-occipital extrastriate regions were accompanied by clusters in the Superior and Inferior Parietal cortex, which were as opposed to the hand gestures also most prominent on the right side. In contrast, hand gestures exclusively activated homologous regions in the left inferior parietal cortex. The authors suggested that this parietal activity might reflect the imitation and preparation for action (see also de Gelder, 2006; Decety & Grèzes, 1999; Goodale & Milner, 1992; Grezes et al., 1998).
Accordingly, the present results may point to a higher demand for action when subjects are confronted with insulting hand gestures indicating a possible threat and thus being of imminent behavioral relevance.
Even though the present results closely match a priori expectations derived from previous research, the absence of differential activation specifically in affective cortical and sub-cortical networks remains puzzling. Particularly, it has been proposed that increased activation in sensory cortical areas while viewing emotional materials would be secondary to enhanced amygdala responses (see Davis & Whalen, 2001; de
Gelder, 2006; Junghöfer et al., 2005; Sabatinelli et al., 2005; Vuilleumier, 2002).
However, recent EEG studies examining the habituation of emotion selective processing showed that the observed ERP effects did not habituate (Schupp et al., 2006). These results are in disagreement with brain imaging studies demonstrating rather quick habituation of amygdala activity while viewing emotional faces (Breiter et al., 1996; Whalen et al., 1998; Wright et al., 2001). Therefore, emotion selective processing particularly in associative sensory cortex may not be completely dependent on input from the amygdala. Other reasons for the absence of according activations may be related to methodological issues. In the present study, a block design incorporating rather long epochs being comprised of many separate picture presentations was utilized. Whereas relatively transient activity in affective networks may have habituated during the course of a stimulation block, activity in associative visual cortex may be comparably more long-lasting, in effect contributing much more experimental variance to the statistical model. Moreover, the sensitivity of the utilized scanning procedure may have been insufficient to detect BOLD modulations in small sub-cortical structures. Therefore, based on the present data it cannot be ruled out that responses in affective cortical and sub-cortical networks may also be elicited by emotional hand gestures. This will have to be clarified by further studies implementing event-related designs and using optimized scanning sequences.
In sum, the present study demonstrates enhanced neuronal encoding of emotional hand gestures with highly symbolic meaning. Emotional as compared to neutral gestures were accompanied by increased BOLD activity in associative visual and parietal cortex. Relating to previous studies using facial expressions and emotional body language, this effect was most pronounced for insulting gestures, signaling potential threat and immediate danger. The present results suggest that the significance of emotional stimuli eliciting selective processing in the brain does not only reflect our biological heritage but may also get attached to highly symbolic stimuli by means of social learning.