Processing of disgusted faces is facilitated by odor primes: A functional MRI study

Department of Psychiatry and Psychotherapy, RWTH Aachen University, Aachen, Germany.
NeuroImage (Impact Factor: 6.36). 11/2010; 53(2):746-56. DOI: 10.1016/j.neuroimage.2010.07.012
Source: PubMed


Facilitation of emotional face recognition is an established phenomenon for audiovisual crossmodal stimulation, but not for other sensory modalities. The present study used a crossmodal priming task to identify brain systems controlling olfactory-visual interactions during emotion processing. BOLD fMRI was acquired for 44 healthy subjects during an emotional face discrimination task preceded by an emotionally valenced odorant. Behavioral performance showed that recognition of disgusted faces was improved by the presentation of an olfactory stimulus irrespective of its emotional valence. No such facilitation was seen for other facial expressions. The neuroimaging data showed a selective default network responsivity to emotional faces which was modulated by odor condition. Among disgust faces, hypoactivations during trials preceded by odorants indicated the presence of priming effects. Consistent with studies investigating the brain systems associated with audiovisual emotional integration, activity modulations in clusters in fusiform gyrus, middle frontal and middle cingulate gyrus corresponded to the observed behavioral facilitation. Our study further shows modulation of signal in the anterior insula during trials combining negatively valenced odor and disgusted faces, suggesting a modality-specific mechanism for integration of the disgust response and olfaction. These results indicate the presence of a central network with modality-specific and -unspecific components modulating emotional face recognition.

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    • "To note, our design of paired (congruent or incongruent) stimulation helped to circumvent the challenge in selecting statistical criteria for fMRI assessment of multisensory integration, due to the inadequate spatial resolution of fMRI for isolating multimodal versus unimodal neurons (Beauchamp, 2005; Goebel and van Atteveldt, 2009; Watson et al., 2014). Specifically, as adopted by several prior studies (Dolan et al., 2001; Ethofer et al., 2006a; Seubert et al., 2010; Forscher and Li, 2012), the contrasts between congruent (negative–negative) versus incongruent (negative– neutral) pairings here overcame the criterion predicament by assuming that " a distinction between congruent and incongruent cross-modal stimulus pairs cannot be established unless the unimodal inputs have been integrated successfully " (Goebel and van Atteveldt, 2009). "
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    • "Conversely, Seubert et al. (2010b) identified slower and less accurate recognition of smiling faces with odor priming regardless of the valence of the odor (vanillin vs. hydrogen sulfide), but enhanced speed and accuracy for disgust faces. An fMRI study demonstrated that odorants activate the primary olfactory cortex, the anterior insula and the superior temporal gyrus during the perception of facial expressions (Seubert et al., 2010a). Hypoactivation for disgust faces in the fusiform, middle frontal and middle cingulate gyri was interpreted as reflecting the priming effect of both aversive and pleasant odorants. "
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    ABSTRACT: We studied the time course of the cerebral integration of olfaction in the visual processing of emotional faces during an orthogonal task asking for detection of red-colored faces among expressive faces. Happy, angry, disgust, fearful, sad, and neutral faces were displayed in pleasant, aversive or no odor control olfactory contexts while EEG was recorded to extract event-related potentials (ERPs). Results indicated that the expressive faces modulated the cerebral responses at occipito-parietal, central and central-parietal electrodes from around 100 ms and until 480 ms after face onset. The response was divided in different successive stages corresponding to different ERP components (P100, N170, P200 and N250 (EPN), and LPP). The olfactory contexts influenced the ERPs in response to facial expressions in two phases. First, regardless of their emotional content, the response to faces was enhanced by both odors compared with no odor approximately 160 ms after face-onset at several central, centro-parietal and left lateral electrodes. The topography of this effect clearly depended on the valence of odors. Then, a second phase occurred, but only in the aversive olfactory context, which modulated differentially the P200 at occipital sites (starting approximately 200ms post-stimulus) by amplifying the differential response to expressions, especially between emotional neutrality and both happiness and disgust. Overall, the present study suggests that the olfactory context first elicits an undifferentiated effect around 160ms after face onset, followed by a specific modulation at 200ms induced by the aversive odor on neutral and affectively congruent/incongruent expressions.
    Neuropsychologia 09/2015; DOI:10.1016/j.neuropsychologia.2015.09.014 · 3.30 Impact Factor
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    • "Only recently, however, studies have begun to experimentally explore the mechanisms by which odors exert an influence on visual perception. In line with experimental evidence indicating that the emotional valence of olfactory cues can affect preference for previously neutral visual stimuli [5], [6], [7], [8], or emotion identification performance [9], [10], [11], studies have demonstrated that the perception of the attractiveness of facial features can be modulated by concurrent presentation of odors with either a very positive or very negative valence [12], [13]. Whether these effects are specific to affective processing, however, remains to be explored. "
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    ABSTRACT: Scented cosmetic products are used across cultures as a way to favorably influence one's appearance. While crossmodal effects of odor valence on perceived attractiveness of facial features have been demonstrated experimentally, it is unknown whether they represent a phenomenon specific to affective processing. In this experiment, we presented odors in the context of a face battery with systematic feature manipulations during a speeded response task. Modulatory effects of linear increases of odor valence were investigated by juxtaposing subsequent memory-based ratings tasks - one predominantly affective (attractiveness) and a second, cognitive (age). The linear modulation pattern observed for attractiveness was consistent with additive effects of face and odor appraisal. Effects of odor valence on age perception were not linearly modulated and may be the result of cognitive interference. Affective and cognitive processing of faces thus appear to differ in their susceptibility to modulation by odors, likely as a result of privileged access of olfactory stimuli to affective brain networks. These results are critically discussed with respect to potential biases introduced by the preceding speeded response task.
    PLoS ONE 05/2014; 9(5):e98347. DOI:10.1371/journal.pone.0098347 · 3.23 Impact Factor
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