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

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.

[1]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[2]  P. Jurs,et al.  Intranasal trigeminal stimulation from odorous volatiles: Psychometric responses from anosmic and normal humans , 1978, Physiology & Behavior.

[3]  E. Stein,et al.  Cingulate activation increases dynamically with response speed under stimulus unpredictability. , 2007, Cerebral cortex.

[4]  F. Gosselin,et al.  Audio-visual integration of emotion expression , 2008, Brain Research.

[5]  R. Sperry,et al.  Lateralization of olfactory perception in the surgically separated hemispheres of man , 1969 .

[6]  J. Hietanen,et al.  Affect and face perception: odors modulate the recognition advantage of happy faces. , 2003, Emotion.

[7]  P. Lang The Cognitive Psychophysiology of Emotion , 2019, Anxiety and the Anxiety Disorders.

[8]  A. Anderson,et al.  Positive affect increases the breadth of attentional selection , 2007, Proceedings of the National Academy of Sciences.

[9]  U. Habel,et al.  Multisensory integration of emotionally valenced olfactory-visual information in patients with schizophrenia and healthy controls. , 2010, Journal of psychiatry & neuroscience : JPN.

[10]  M. Bradley,et al.  Both Predator and Prey , 2008, Psychological science.

[11]  B. Fredrickson The broaden-and-build theory of positive emotions. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  A. Fallon,et al.  A perspective on disgust. , 1987, Psychological review.

[13]  Michael Erb,et al.  Audiovisual integration of emotional signals in voice and face: An event-related fMRI study , 2007, NeuroImage.

[14]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[15]  R. Gur,et al.  Neural circuitry for accurate identification of facial emotions , 2008, Brain Research.

[16]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[17]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[18]  K. Berridge,et al.  Towards a functional neuroanatomy of pleasure and happiness , 2009, Trends in Cognitive Sciences.

[19]  M. Jones-Gotman,et al.  The human brain distinguishes between single odorants and binary mixtures. , 2009, Cerebral cortex.

[20]  J. Maser,et al.  Anxiety and the Anxiety Disorders , 2019 .

[21]  K. Scherer,et al.  Evidence for universality and cultural variation of differential emotion response patterning. , 1994, Journal of personality and social psychology.

[22]  Gerd Kobal,et al.  Screening of Olfactory Function with a Four-Minute Odor Identification Test: Reliability, Normative Data, and Investigations in Patients with Olfactory Loss , 2001, The Annals of otology, rhinology, and laryngology.

[23]  J. Price,et al.  Central olfactory connections in the macaque monkey , 1994, The Journal of comparative neurology.

[24]  B. Stein,et al.  Interactions among converging sensory inputs in the superior colliculus. , 1983, Science.

[25]  Narayanan Srinivasan,et al.  Time course of visual attention with emotional faces , 2010, Attention, perception & psychophysics.

[26]  P. Bertelson,et al.  The ventriloquist effect does not depend on the direction of deliberate visual attention , 2000, Perception & psychophysics.

[27]  W. Goodman,et al.  Disgust and the insula: fMRI responses to pictures of mutilation and contamination , 2004, Neuroreport.

[28]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

[29]  A. Young,et al.  Impaired recognition and experience of disgust following brain injury , 2000, Nature Neuroscience.

[30]  Robin M. Chan,et al.  An fMRI study of facial emotion processing in patients with schizophrenia. , 2002, The American journal of psychiatry.

[31]  D. Schacter,et al.  Reductions in cortical activity during priming , 2007, Current Opinion in Neurobiology.

[32]  Bridget M Waller,et al.  Selection for universal facial emotion. , 2008, Emotion.

[33]  J. Vroomen,et al.  Sound enhances visual perception: cross-modal effects of auditory organization on vision. , 2000, Journal of experimental psychology. Human perception and performance.

[34]  P. Ekman,et al.  Constants across cultures in the face and emotion. , 1971, Journal of personality and social psychology.

[35]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[36]  James M Kilner,et al.  Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala , 2005, The Journal of Neuroscience.

[37]  G Kobal,et al.  Olfactory functional imaging and physiology. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  S. Campanella,et al.  Integrating face and voice in person perception , 2007, Trends in Cognitive Sciences.

[39]  Nobuyuki Sakai,et al.  Functional MRI of regional brain responses to ‘pleasant’ and ‘unpleasant’ odors , 2009, Acta oto-laryngologica. Supplementum.

[40]  Raymond J. Dolan,et al.  Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence , 2005, NeuroImage.

[41]  Michael Erb,et al.  Impact of voice on emotional judgment of faces: An event‐related fMRI study , 2006, Human brain mapping.

[42]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[43]  J. Hietanen,et al.  Judgment of other people's facial expressions of emotions is influenced by their concurrent affective hand movements. , 2008, Scandinavian journal of psychology.

[44]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[45]  R. Stevenson,et al.  Disgust as a disease-avoidance mechanism. , 2009, Psychological bulletin.

[46]  Jon Driver,et al.  Is cross-modal integration of emotional expressions independent of attentional resources? , 2001, Cognitive, affective & behavioral neuroscience.

[47]  R. Gur,et al.  Facial emotion recognition in schizophrenia: intensity effects and error pattern. , 2003, The American journal of psychiatry.

[48]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[49]  Nico Bunzeck,et al.  Category-specific organization of prefrontal response-facilitation during priming , 2006, Neuropsychologia.

[50]  C Caltagirone,et al.  Brain activity during intra- and cross-modal priming: new empirical data and review of the literature , 2004, Neuropsychologia.

[51]  J. Royet,et al.  Lateralization of olfactory processes. , 2004, Chemical senses.

[52]  Julie Grèzes,et al.  Human and animal sounds influence recognition of body language , 2008, Brain Research.

[53]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[54]  Janina Seubert,et al.  Mood induction with olfactory stimuli reveals differential affective responses in males and females. , 2008, Chemical senses.

[55]  Species-specific defense reactions and avoidance learning. An evaluative review. , 1982, The Pavlovian journal of biological science.