An evil face? Verbal evaluative multi-CS conditioning enhances face-evoked mid-latency magnetoencephalographic responses

Abstract Humans have a remarkable capacity for rapid affective learning. For instance, using first-order US such as odors or electric shocks, magnetoencephalography (MEG) studies of multi-CS conditioning demonstrate enhanced early (<150 ms) and mid-latency (150–300 ms) visual evoked responses to affectively conditioned faces, together with changes in stimulus evaluation. However, particularly in social contexts, human affective learning is often mediated by language, a class of complex higher-order US. To elucidate mechanisms of this type of learning, we investigate how face processing changes following verbal evaluative multi-CS conditioning. Sixty neutral expression male faces were paired with phrases about aversive crimes (30) or neutral occupations (30). Post conditioning, aversively associated faces evoked stronger magnetic fields in a mid-latency interval between 220 and 320 ms, localized primarily in left visual cortex. Aversively paired faces were also rated as more arousing and more unpleasant, evaluative changes occurring both with and without contingency awareness. However, no early MEG effects were found, implying that verbal evaluative conditioning may require conceptual processing and does not engage rapid, possibly sub-cortical, pathways. Results demonstrate the efficacy of verbal evaluative multi-CS conditioning and indicate both common and distinct neural mechanisms of first- and higher-order multi-CS conditioning, thereby informing theories of associative learning.

[1]  Gregory A. Miller,et al.  Distinguishing Dimensions of Anxiety and Depression , 2001, Cognitive Therapy and Research.

[2]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[3]  E. Phelps,et al.  Social learning of fear , 2007, Nature Neuroscience.

[4]  M. Perugini,et al.  Evaluative conditioning in humans: a meta-analysis. , 2010, Psychological bulletin.

[5]  C. Staats,et al.  Meaning established by classical conditioning. , 1957, Journal of experimental psychology.

[6]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[7]  T. Wickens Elementary Signal Detection Theory , 2001 .

[8]  Jeff T. Larsen,et al.  Context dependence of the event-related brain potential associated with reward and punishment. , 2004, Psychophysiology.

[9]  Richard J Davidson,et al.  Spatio-temporal dynamics of brain mechanisms in aversive classical conditioning: high-density event-related potential and brain electrical tomography analyses , 2003, Neuropsychologia.

[10]  S. Baldassi,et al.  Fearful expressions enhance recognition memory: electrophysiological evidence. , 2012, Acta psychologica.

[11]  E. Walther Guilty by mere association: evaluative conditioning and the spreading attitude effect. , 2002, Journal of personality and social psychology.

[12]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[13]  Matthias M. Müller,et al.  Emotional words facilitate lexical but not early visual processing , 2015, BMC Neuroscience.

[14]  Mark Warr,et al.  Fear of Crime in the United States: Avenues for Research and Policy , 2000 .

[15]  R. Balas,et al.  Evaluative conditioning may occur with and without contingency awareness , 2012, Psychological research.

[16]  Andreas Olsson,et al.  Learned Fear of “Unseen” Faces after Pavlovian, Observational, and Instructed Fear , 2004, Psychological science.

[17]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

[18]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[19]  M. Junghöfer,et al.  Affect‐specific modulation of the N1m to shock‐conditioned tones: magnetoencephalographic correlates , 2013, The European journal of neuroscience.

[20]  Ann-Kathrin Bröckelmann,et al.  Rapid and highly resolving associative affective learning: Convergent electro- and magnetoencephalographic evidence from vision and audition , 2013, Biological Psychology.

[21]  Sara L Bryson,et al.  Fear of crime in the United States , 2016 .

[22]  L. Kuchinke,et al.  Acquired affective associations induce emotion effects in word recognition: An ERP study , 2013, Brain and Language.

[23]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[24]  Olaf Steinsträter,et al.  Sensitivity of beamformer source analysis to deficiencies in forward modeling , 2010, Human brain mapping.

[25]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[26]  Pienie Zwitserlood,et al.  Rapid Plasticity in the Prefrontal Cortex during Affective Associative Learning , 2014, PloS one.

[27]  Urs Maurer,et al.  The face-specific N170 component is modulated by emotional facial expression , 2007, Behavioral and Brain Functions.

[28]  Markus Junghöfer,et al.  Evidence for rapid prefrontal emotional evaluation from visual evoked responses to conditioned gratings , 2014, Biological Psychology.

[29]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.

[30]  J. Kissler The Cambridge Handbook of Human Affective Neuroscience: Love Letters and Hate Mail , 2013 .

[31]  Michael A. Olson,et al.  Reducing Automatically Activated Racial Prejudice Through Implicit Evaluative Conditioning , 2006, Personality & social psychology bulletin.

[32]  Skyler T. Hawk,et al.  Presentation and validation of the Radboud Faces Database , 2010 .

[33]  Christoph M. Michel,et al.  Two electrophysiological stages of spatial orienting towards fearful faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex , 2005, NeuroImage.

[34]  JAN DEHOUWER,et al.  Verbal evaluative conditioning with undetected US presentations , 2022 .

[35]  A. Chaudhuri,et al.  The Many Faces of a Neutral Face: Head Tilt and Perception of Dominance and Emotion , 2003 .

[36]  Søren K. Andersen,et al.  Capture of lexical but not visual resources by task-irrelevant emotional words: A combined ERP and steady-state visual evoked potential study , 2012, NeuroImage.

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

[38]  Wolfgang Grodd,et al.  Amygdala activation during reading of emotional adjectives--an advantage for pleasant content. , 2009, Social cognitive and affective neuroscience.

[39]  U. Dimberg,et al.  Facial reactions, autonomic activity and experienced emotion: A three component model of emotional conditioning , 1987, Biological Psychology.

[40]  Tobias Brosch,et al.  Beyond Fear , 2008, Psychological science.

[41]  Taomei Guo,et al.  Association with positive outcome induces early effects in event-related brain potentials , 2012, Biological Psychology.

[42]  A. Sanfey,et al.  Independent Coding of Reward Magnitude and Valence in the Human Brain , 2004, The Journal of Neuroscience.

[43]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[44]  K. C. Klauer,et al.  Dissociating contingency awareness and conditioned attitudes: evidence of contingency-unaware evaluative conditioning. , 2012, Journal of experimental psychology. General.

[45]  Rachael E. Jack,et al.  Internal representations reveal cultural diversity in expectations of facial expressions of emotion. , 2012, Journal of experimental psychology. General.

[46]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[47]  Francesca M. M. Citron Neural correlates of written emotion word processing: A review of recent electrophysiological and hemodynamic neuroimaging studies , 2012, Brain and Language.

[48]  Cornelia Herbert,et al.  Emotion, Etmnooi, or Emitoon? – Faster lexical access to emotional than to neutral words during reading , 2013, Biological Psychology.

[49]  A. Staats,et al.  Meaning and m: correlated but separate. , 1959, Psychological review.

[50]  Pienie Zwitserlood,et al.  Rapid prefrontal cortex activation towards aversively paired faces and enhanced contingency detection are observed in highly trait-anxious women under challenging conditions , 2015, Front. Behav. Neurosci..

[51]  A. Ohman,et al.  Automaticity and the Amygdala: Nonconscious Responses to Emotional Faces , 2002 .

[52]  W. Sommer,et al.  Interplay of emotional valence and concreteness in word processing: An event-related potential study with verbs , 2013, Brain and Language.

[53]  Rasha Abdel Rahman,et al.  Facing good and evil: early brain signatures of affective biographical knowledge in face recognition. , 2011, Emotion.

[54]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[55]  Amy Wrzesniewski,et al.  Odors can change preferences for people in photographs: A cross-modal evaluative conditioning study with olfactory USs and visual CSs , 1995 .

[56]  F. Baeyens,et al.  Evaluative Learning with “Subliminally” Presented Stimuli , 1997, Consciousness and Cognition.

[57]  N Birbaumer,et al.  Cortical correlates of semantic classical conditioning. , 1996, Psychophysiology.

[58]  Christo Pantev,et al.  Emotion-Associated Tones Attract Enhanced Attention at Early Auditory Processing: Magnetoencephalographic Correlates , 2011, The Journal of Neuroscience.

[59]  A. Mecklinger,et al.  Recognition Memory for Emotional and Neutral Faces: An Event-Related Potential Study , 2004, Journal of Cognitive Neuroscience.

[60]  W. Miltner,et al.  Brain activation to briefly presented emotional words: Effects of stimulus awareness , 2015, Human brain mapping.

[61]  L. Kuchinke,et al.  Evaluative conditioning of positive and negative valence affects P1 and N1 in verbal processing , 2015, Brain Research.

[62]  J. Kissler,et al.  Buzzwords , 2007, Psychological science.

[63]  D. Grandjean,et al.  Electrophysiological correlates of rapid spatial orienting towards fearful faces. , 2004, Cerebral cortex.

[64]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

[65]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[66]  G. Crombez,et al.  Expectancy-learning and evaluative learning in human classical conditioning: affective priming as an indirect and unobtrusive measure of conditioned stimulus valence. , 2002, Behaviour research and therapy.

[67]  Olaf Hauk,et al.  Keep it simple: a case for using classical minimum norm estimation in the analysis of EEG and MEG data , 2004, NeuroImage.

[68]  L. Cahill Why sex matters for neuroscience , 2006, Nature Reviews Neuroscience.

[69]  J. Kissler,et al.  Emotion and attention in visual word processing—An ERP study , 2009, Biological Psychology.

[70]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[71]  Christo Pantev,et al.  Rapid and Highly Resolving: Affective Evaluation of Olfactorily Conditioned Faces , 2012, Journal of Cognitive Neuroscience.

[72]  J. de Houwer,et al.  Associative learning of likes and dislikes: a review of 25 years of research on human evaluative conditioning. , 2001, Psychological bulletin.

[73]  L. Laux,et al.  Das State-Trait-Angstinventar. Theoretische Grundlagen and Handanweisung. , 1981 .

[74]  J. Armony,et al.  The Cambridge Handbook of Human Affective Neuroscience: Contents , 2013 .

[75]  M. Junghöfer,et al.  Abnormal, affect-specific modulatory effects on early auditory processing in schizophrenia: Magnetoencephalographic evidence , 2015, Schizophrenia Research.

[76]  M. Schmitt,et al.  Vorschlag zur Vereinfachung des Beck-Depressions-Inventars (BDI) , 2000 .

[77]  M. Junghöfer,et al.  The facilitated processing of threatening faces: an ERP analysis. , 2004, Emotion.