Neural mechanisms of processing emotional information from faces and voices in social phobia

• Applicants: Professor Dr. Wolfgang Miltner; Professor Dr. Thomas Straube
• Subject Area: Personality Psychology, Clinical and Medical Psychology, Methodology ; General, Cognitive and Mathematical Psychology
• Term: from 2009 to 2017
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 69199027

• Final Report Year: 2017

Final Report Abstract

Several lines of research propose prioritized processing of threat-related social signals in healthy subjects and, even more pronounced, in patients suffering from social anxiety disorder (SAD). This research project systematically investigated spatio-temporal brain responses to emotional facial and vocal expressions under different attentional conditions in healthy individuals and patients suffering from SAD. In the course of the project, we developed a new battery of suited social stimuli and novel designs for the investigation of attentional effects on the neural correlates of the processing of emotional faces and voices. The analyses of these data yielded several novel findings concerning the role of attention, stimulus intensity and social anxiety for the understanding of neural mechanisms of processing emotional facial expression and prosody. In particular, we revealed that threatening voices are not processed automatically, since both visual and auditory load conditions prevented increased responses in amygdala and auditory cortex to angry vs neutral prosody. Furthermore, we found that intensity but not threat-relevance of facial expressions is associated with amygdala activation. Activation in the amygdala followed a U-shaped function with strongest activation to high intensity angry and happy expressions. Using event-related potentials (ERPs) we also showed that emotional intensity modulates early ERPs to facial expressions regardless of perceptual load. Specifically, the N170 amplitude showed a U-shaped pattern with strongest amplitudes in response to high intensity angry and happy expressions. Currently we further analyze simultaneously acquired fMRI/ERP data for several experiments with emotional faces and voices in healthy individuals and patients with SAD. In a combined EEG-fMRI study using facial expressions varying in emotional intensity, ERP analysis indicated intensity sensitivity within early (100 to 130ms) latencies. Expression effects in the EEG resembled those found in conventional fMRI analysis showing U-shaped response patterns with largest amplitudes for high intensity emotional expressions. On a single trial basis, integrated EEG-fMRI analysis revealed a significant correlation between early EEG activity and specifically occipital face area (rOFA), suggesting early facial expression effects in both temporal and topographical neural responses.We also showed that sound intensity modulates amygdala activation to angry prosody in SAD. Only loud and angry voices differentiated between healthy subjects and patients with SAD. Using ERPs, a further study revealed a sustained attentional bias to behaviorally relevant angry faces in SAD. Taken together, findings clearly show that brain responses to social threat signals are modulated by attentional resources, intensity of stimuli and social anxiety. Brain responses to social threat depend on processing resources, even though effects are less pronounced for early ERPs as compared to late ERPs and fMRI data. Furthermore, at least in healthy subjects, intensity of emotional signals is a better predictor of brain responses than stimulus valence. Finally, patients with SAD show specifically increased brain responses to social threat signals. If stimuli are behaviorally relevant, patients suffering from SAD are characterized by sustained prioritized processing of social threat signals.

Publications

• (2010). The volatility of the amygdala response to masked fearful eyes. Human Brain Mapping, 31(10), 1601-1608
  Straube, T., Dietrich, C., Mothes-Lasch, M., Mentzel, H. J., & Miltner, W. H.
  
• (2011). Neural mechanisms of automatic processing of emotional information from faces and voices. British Journal of Psychology, 102(4), 830-848
  Straube, T., Mothes-Lasch, M., & Miltner, W. H.
  
• (2011). Visual attention modulates brain activation to angry voices. Journal of Neuroscience, 31(26), 9594-9598
  Mothes-Lasch, M., Mentzel, H. J., Miltner, W.H. & Straube, T.
  
• (2012). Processing of angry voices is modulated by visual load. Neuroimage, 63(1), 485-490
  Mothes-Lasch, M., Miltner, W. H., & Straube, T.
  
• (2013). Amygdala activation to fearful faces under attentional load. Behavioral Brain Research, 237, 172-175
  Mothes-Lasch, M., Mentzel, H. J., Miltner, W. H., & Straube, T.
  
• (2013). Automatic neural processing of disorder-related stimuli in social anxiety disorder: faces and more. Frontiers in Psychology, 4, 282
  Schulz, C., Mothes-Lasch, M., & Straube, T.
  
• (2014). Area-dependent time courses of brain activation during video-induced symptom provocation in social anxiety disorder. Biology of Mood & Anxiety Disorders, 4, 6
  Boehme, S., Mohr, A., Becker, M. P., Miltner, W. H., & Straube, T.
  
• (2014). Effects of gaze direction, head orientation, and valence of facial expression on amygdala activity. Social Cognitive and Affective Neuroscience, 9(8), 1246-1252
  Sauer, A., Mothes-Lasch, M., Miltner, W. H., & Straube, T.
  
• (2015). Cognitive tasks during expectation affect the congruency ERP effects to facial expressions. Frontiers in Human Neuroscience, 9, 596
  Lin, H., Schulz, C., & Straube, T.
  
• (2015). Fearful contextual expression impairs the encoding and recognition of target faces: an ERP study. Frontiers in Behavioral Neuroscience, 9, 237
  Lin, H., Schulz, C., & Straube, T.
  
• (2015). Neural correlates of self-focused attention in social anxiety. Social Cognitive and Affective Neuroscience, 10(6), 856-862
  Boehme, S., Miltner, W. H., & Straube, T.
  
• (2016). Abnormal brain activation and connectivity to standardized disorder-related visual scenes in social anxiety disorder. Human Brain Mapping, 37(4), 1559-1572
  Heitmann, C. Y., Feldker, K., Neumeister, P., Zepp, B. M., Peterburs, J., Zwitserlood, P., & Straube, T.
  
• (2016). Effects of emotional intensity under perceptual load: An event-related potentials (ERPs) study. Biological Psychology, 117, 141-149
  Müller-Bardorff, M., Schulz, C., Peterburs, J., Bruchmann, M., Mothes-Lasch, M., Miltner, W., & Straube, T.
  
• (2016). Effects of expectation congruency on event-related potentials (ERPs) to facial expressions depend on cognitive load during the expectation phase. Biological Psychology, 120, 126-136
  Lin, H., Schulz, C., & Straube, T.
  
• (2016). Effects of Intensity of Facial Expressions on Amygdalar Activation Independently of Valence. Frontiers in Human Neuroscience, 10, 646
  Lin, H., Müller-Bardorff, M., Mothes-Lasch, M., Buff, C., Brinkmann, L., Miltner, W. H., & Straube, T.
  
• (2016). Neural basis of processing threatening voices in a crowded auditory world. Social Cognitive and Affective Neuroscience, 11(5), 821-828
  Mothes-Lasch, M., Becker, M. P., Miltner, W. H., & Straube, T.
  
• (2016). Too bad: Bias for angry faces in social anxiety interferes with identity processing. Neuropsychologia, 84, 136-149
  Hagemann, J., Straube, T., & Schulz, C.
  
• (2017). Loud and angry: Sound intensity modulates amygdala activation to angry voices in social anxiety disorder. Social Cognitive and Affective Neuroscience, 12, 409-416
  Simon, D., Becker, M. P., Mothes-Lasch, M., Miltner, W. H., & Straube, T.