The implicit processing of categorical and dimensional strategies: an fMRI study of facial emotion perception

Our understanding of facial emotion perception has been dominated by two seemingly opposing theories: the categorical and dimensional theories. However, we have recently demonstrated that hybrid processing involving both categorical and dimensional perception can be induced in an implicit manner (Fujimura etal., 2012). The underlying neural mechanisms of this hybrid processing remain unknown. In this study, we tested the hypothesis that separate neural loci might intrinsically encode categorical and dimensional processing functions that serve as a basis for hybrid processing. We used functional magnetic resonance imaging to measure neural correlates while subjects passively viewed emotional faces and performed tasks that were unrelated to facial emotion processing. Activity in the right fusiform face area (FFA) increased in response to psychologically obvious emotions and decreased in response to ambiguous expressions, demonstrating the role of the FFA in categorical processing. The amygdala, insula and medial prefrontal cortex exhibited evidence of dimensional (linear) processing that correlated with physical changes in the emotional face stimuli. The occipital face area and superior temporal sulcus did not respond to these changes in the presented stimuli. Our results indicated that distinct neural loci process the physical and psychological aspects of facial emotion perception in a region-specific and implicit manner.

[1]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[2]  Alumit Ishai,et al.  Face Perception Is Modulated by Sexual Preference , 2006, Current Biology.

[3]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

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

[5]  G. A. Mendelsohn,et al.  Affect grid : A single-item scale of pleasure and arousal , 1989 .

[6]  John J. Magee,et al.  Categorical perception of facial expressions , 1992, Cognition.

[7]  Michel Baudry,et al.  The amygdala modulates prefrontal cortex activity relative to conditioned fear , 1999, Nature.

[8]  H. Schlosberg.  Three dimensions of emotion. , 1954, Psychological review.

[9]  J. Russell.  A circumplex model of affect. , 1980 .

[10]  Leslie G. Ungerleider,et al.  Repetition suppression of faces is modulated by emotion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[11]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[12]  Matthias J. Wieser,et al.  Brain Activations to Emotional Pictures are Differentially Associated with Valence and Arousal Ratings , 2010, Front. Hum. Neurosci..

[13]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[14]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  J. Pardo,et al.  Elucidating Dynamic Brain Interactions with Across-Subjects Correlational Analyses of Positron Emission Tomographic Data: The Functional Connectivity of the Amygdala and Orbitofrontal Cortex during Olfactory Tasks , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[16]  Kenneth F. Valyear,et al.  The involvement of the “fusiform face area” in processing facial expression , 2005, Neuropsychologia.

[17]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[18]  A. Young,et al.  Understanding the recognition of facial identity and facial expression , 2005, Nature Reviews Neuroscience.

[19]  M. Seghier,et al.  A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. , 2003, Brain : a journal of neurology.

[20]  Ariel Woodbury,et al.  How do you feel? , 2014, Nursing.

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

[22]  D. Perrett,et al.  Facial expression megamix: Tests of dimensional and category accounts of emotion recognition , 1997, Cognition.

[23]  Georgia Panayiotou,et al.  Emotional dimensions reflected in ratings of affective scripts , 2008 .

[24]  Bruno Rossion,et al.  Understanding the functional neuroanatomy of acquired prosopagnosia , 2007, NeuroImage.

[25]  T. Allison,et al.  Brain activation evoked by perception of gaze shifts: the influence of context , 2003, Neuropsychologia.

[26]  N. Kanwisher,et al.  The Neural Basis of the Behavioral Face-Inversion Effect , 2005, Current Biology.

[27]  Marco Tamietto,et al.  Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions , 2010, Neuroscience & Biobehavioral Reviews.

[28]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[29]  Tom Johnstone,et al.  Regional response differences across the human amygdaloid complex during social conditioning. , 2010, Cerebral cortex.

[30]  N. Kanwisher,et al.  The fusiform face area: a cortical region specialized for the perception of faces , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  P. Ekman.  An argument for basic emotions , 1992 .

[32]  Clinton D. Kilts,et al.  Dissociable Neural Pathways Are Involved in the Recognition of Emotion in Static and Dynamic Facial Expressions , 2003, NeuroImage.

[33]  G. Pagnoni,et al.  Explicit and Incidental Facial Expression Processing: An fMRI Study , 2001, NeuroImage.

[34]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

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

[36]  R. Davidson.  Anxiety and affective style: role of prefrontal cortex and amygdala , 2002, Biological Psychiatry.

[37]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[38]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[39]  P. Lang.  International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[40]  M. Trimble,et al.  The Human Amygdala , 2010 .

[41]  Christopher J. Fox,et al.  Defining the face processing network: Optimization of the functional localizer in fMRI , 2009, Human brain mapping.

[42]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[43]  D. Perrett,et al.  Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness , 2003, Neuropsychologia.

[44]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[45]  Raymond J. Dolan,et al.  Face adaptation aftereffects reveal anterior medial temporal cortex role in high level category representation , 2007, NeuroImage.

[46]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[47]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[48]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[49]  Thomas J. Ross,et al.  Amygdala response to both positively and negatively valenced stimuli , 2001, Neuroreport.

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

[51]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[52]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[53]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[54]  N. Alpert,et al.  Activation of anterior paralimbic structures during guilt-related script-driven imagery , 2000, Biological Psychiatry.

[55]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[56]  A. Anderson,et al.  Facial expression form and function , 2008, Communicative & integrative biology.

[57]  Giuseppe Iaria,et al.  The correlates of subjective perception of identity and expression in the face network: An fMRI adaptation study , 2009, NeuroImage.

[58]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[59]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

[60]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[61]  M. Phillips,et al.  A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder , 2008, Molecular Psychiatry.

[62]  Alumit Ishai,et al.  Let’s face it: It’s a cortical network , 2008, NeuroImage.

[63]  Christian Büchel,et al.  The influence of directed covert attention on emotional face processing , 2010, NeuroImage.

[64]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[65]  D. Paré,et al.  Prefrontal Control of the Amygdala , 2005, The Journal of Neuroscience.

[66]  G. Rhodes,et al.  Are you always on my mind? A review of how face perception and attention interact , 2007, Neuropsychologia.

[67]  John S Morrisj.  How do you feel? , 2002, Trends in Cognitive Sciences.

[68]  Ralph Adolphs,et al.  The neuropsychology of face perception: beyond simple dissociations and functional selectivity , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[70]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[71]  M. Katsikitis,et al.  The Classification of Facial Expressions of Emotion: A Multidimensional-Scaling Approach , 1997, Perception.

[72]  James A. Russell,et al.  Multidimensional scaling of emotional facial expressions: Similarity from preschoolers to adults. , 1985 .

[73]  D. Paré,et al.  Stimulation of Medial Prefrontal Cortex Decreases the Responsiveness of Central Amygdala Output Neurons , 2003, The Journal of Neuroscience.

[74]  Giuseppe Iaria,et al.  Disconnection in prosopagnosia and face processing , 2008, Cortex.

[75]  Hongtu Zhu,et al.  An affective circumplex model of neural systems subserving valence, arousal, and cognitive overlay during the appraisal of emotional faces , 2008, Neuropsychologia.

[76]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[77]  K. Katahira,et al.  Categorical and dimensional perceptions in decoding emotional facial expressions , 2011, Cognition & emotion.

[78]  Á. Pascual-Leone,et al.  How do we modulate our emotions? Parametric fMRI reveals cortical midline structures as regions specifically involved in the processing of emotional valences. , 2005, Brain research. Cognitive brain research.

[79]  Christian Büchel,et al.  Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans , 2010, Proceedings of the National Academy of Sciences.

[80]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[81]  D. Pitcher,et al.  The role of the occipital face area in the cortical face perception network , 2011, Experimental Brain Research.

[82]  Tom Johnstone,et al.  Inverse amygdala and medial prefrontal cortex responses to surprised faces , 2003, Neuroreport.

[83]  I. Christie,et al.  Autonomic specificity of discrete emotion and dimensions of affective space: a multivariate approach. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[84]  D. Perrett,et al.  Categorical Perception of Morphed Facial Expressions , 1996 .

[85]  P. Ekman,et al.  Pan-Cultural Elements in Facial Displays of Emotion , 1969, Science.

[86]  Geoffrey J. McLachlan,et al.  Mixture models : inference and applications to clustering , 1989 .

[87]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[88]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[89]  Carl Senior,et al.  Dynamic Facial Expressions Evoke Distinct Activation in the Face Perception Network: A Connectivity Analysis Study , 2012, Journal of Cognitive Neuroscience.

[90]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[91]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[92]  J. Cacioppo,et al.  Relationship between attitudes and evaluative space: A critical review, with emphasis on the separability of positive and negative substrates. , 1994 .

[93]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[94]  S. Tomkins,et al.  What and Where are the Primary Affects? Some Evidence for a Theory , 1964, Perceptual and motor skills.

[95]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[96]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[97]  E. Rosch,et al.  Family resemblances: Studies in the internal structure of categories , 1975, Cognitive Psychology.

[98]  F H Epstein,et al.  Adaptive sensitivity encoding incorporating temporal filtering (TSENSE) † , 2001, Magnetic resonance in medicine.

[99]  Ralph Adolphs,et al.  Processing of the Arousal of Subliminal and Supraliminal Emotional Stimuli by the Human Amygdala , 2003, The Journal of Neuroscience.

[100]  R. Dolan,et al.  fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. , 2004, Journal of neurophysiology.

[101]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[102]  J. Russell.  Core affect and the psychological construction of emotion. , 2003, Psychological review.

[103]  M. Erb,et al.  Brain activity underlying emotional valence and arousal: A response‐related fMRI study , 2004, Human brain mapping.

[104]  Christopher J. Fox,et al.  What is adapted in face adaptation? The neural representations of expression in the human visual system , 2007, Brain Research.

[105]  Oliver G. B. Garrod,et al.  Facial expressions of emotion are not culturally universal , 2012, Proceedings of the National Academy of Sciences.

[106]  H. Critchley,et al.  Neural correlates of processing valence and arousal in affective words. , 2006, Cerebral cortex.

[107]  Mikko Sams,et al.  Nonlinear relationship between emotional valence and brain activity: Evidence of separate negative and positive valence dimensions , 2009, Human brain mapping.

[108]  R. Dolan,et al.  Separate Coding of Different Gaze Directions in the Superior Temporal Sulcus and Inferior Parietal Lobule , 2007, Current Biology.

[109]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[110]  J. Schwerdtner,et al.  fMRI an der Forensischen Klinik am Bezirksklinikum Regensburg - Neuroanatomische Grundlagen der Emotionsverarbeitung , 2004 .

[111]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[112]  Richard J. Harris,et al.  Morphing between expressions dissociates continuous from categorical representations of facial expression in the human brain , 2012, Proceedings of the National Academy of Sciences.

[113]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[114]  P. Ekman.  Pictures of Facial Affect , 1976 .

[115]  N. Suzuki,et al.  Morphed Images of Basic Emotional Expressions: Ratings on Russell's Bipolar Field , 1997, Perceptual and motor skills.

[116]  J. Russell,et al.  The neurophysiological bases of emotion: An fMRI study of the affective circumplex using emotion‐denoting words , 2009, Human brain mapping.

[117]  E. Naito,et al.  Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. , 2004, Brain research. Cognitive brain research.

[118]  P. Johnson-Laird,et al.  Basic emotions, rationality, and folk theory , 1992 .

[119]  Francesco Versace,et al.  Pleasure rather than salience activates human nucleus accumbens and medial prefrontal cortex. , 2007, Journal of neurophysiology.

[120]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[121]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[122]  S. Schweinberger,et al.  Expression Influences the Recognition of Familiar Faces , 2004, Perception.

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

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

[125]  William A. Cunningham,et al.  Implicit and Explicit Evaluation: fMRI Correlates of Valence, Emotional Intensity, and Control in the Processing of Attitudes , 2004, Journal of Cognitive Neuroscience.

[126]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[127]  David I. Perrett,et al.  Facial expressions of emotion: Stimuli and tests (FEEST) , 2002 .

[128]  S. Corkin,et al.  Two routes to emotional memory: distinct neural processes for valence and arousal. , 2004, Proceedings of the National Academy of Sciences of the United States of America.