Emotion Perception and Elicitation

Over the last 20 years, neuroimaging research in humans has progressively charted emotions on neural activity within distributed and interactive networks of brain regions. This work provides compelling evidence that emotional perception and elicitation are intimately intertwined with a broad range of mental functions, challenging a classic divide between cognitive and affective sectors of the mind. This article describes neural systems engaged by different types of emotional stimuli (e.g., faces, voices, and memories) and different types of emotions (e.g., fear, disgust, and regret). Specificities and commonalities across emotion categories are critically discussed in relation to current theoretical models.

[1]  C. Neuper,et al.  The functional correlates of face perception and recognition of emotional facial expressions as evidenced by fMRI , 2011, Brain Research.

[2]  Dimitri Van De Ville,et al.  White-Matter Connectivity between Face-Responsive Regions in the Human Brain , 2012 .

[3]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

[4]  J. O'Doherty,et al.  Beyond simple reinforcement learning: the computational neurobiology of reward‐learning and valuation , 2012, The European journal of neuroscience.

[5]  A. Damasio Descartes' error: emotion, reason, and the human brain. avon books , 1994 .

[6]  Christian Keysers,et al.  Primary somatosensory cortex discriminates affective significance in social touch , 2012, Proceedings of the National Academy of Sciences.

[7]  Pascal Belin,et al.  Dissociating task difficulty from incongruence in face-voice emotion integration , 2013, Front. Hum. Neurosci..

[8]  Athena Vouloumanos,et al.  The Superior Temporal Sulcus Differentiates Communicative and Noncommunicative Auditory Signals , 2012, Journal of Cognitive Neuroscience.

[9]  M. Just,et al.  Identifying Emotions on the Basis of Neural Activation , 2013, PloS one.

[10]  Peter Boesiger,et al.  Abnormal activity in hypothalamus and amygdala during humour processing in human narcolepsy with cataplexy. , 2008, Brain : a journal of neurology.

[11]  Charles L. Wilson,et al.  Electric current stimulates laughter , 1998, Nature.

[12]  K. Scherer,et al.  Interaction effects of perceived gaze direction and dynamic facial expression: Evidence for appraisal theories of emotion , 2007 .

[13]  J. Russell,et al.  Core affect, prototypical emotional episodes, and other things called emotion: dissecting the elephant. , 1999 .

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

[15]  A. Ishai,et al.  Effective connectivity within the distributed cortical network for face perception. , 2007, Cerebral cortex.

[16]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[17]  Patrik Vuilleumier,et al.  Cognitive and affective theory of mind share the same local patterns of activity in posterior temporal but not medial prefrontal cortex. , 2014, Social cognitive and affective neuroscience.

[18]  G. Pourtois,et al.  Perception of Facial Expressions and Voices and of their Combination in the Human Brain , 2005, Cortex.

[19]  James V. Haxby,et al.  Mirror Neuron System Differentially Activated by Facial Expressions and Social Hand Gestures: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[20]  N. Frijda Impulsive action and motivation , 2010, Biological Psychology.

[21]  Stephan Hamann,et al.  Mapping discrete and dimensional emotions onto the brain: controversies and consensus , 2012, Trends in Cognitive Sciences.

[22]  J. Grafman,et al.  The Human Amygdala: An Evolved System for Relevance Detection , 2003, Reviews in the neurosciences.

[23]  David Sander,et al.  A systems approach to appraisal mechanisms in emotion , 2005, Neural Networks.

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

[25]  A. Young,et al.  Neuropsychology of fear and loathing , 2001 .

[26]  B. Peterson,et al.  Preliminary evidence for persistent abnormalities in amygdala volumes in adolescents and young adults with bipolar disorder. , 2005, Bipolar disorders.

[27]  Jeffrey S. Maxwell,et al.  Human Amygdala Responsivity to Masked Fearful Eye Whites , 2004, Science.

[28]  Wolfgang Grodd,et al.  Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus , 2009, Neuropsychologia.

[29]  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.

[30]  G. Pourtois,et al.  Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging , 2007, Neuropsychologia.

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

[32]  R. Dolan,et al.  Distant influences of amygdala lesion on visual cortical activation during emotional face processing , 2004, Nature Neuroscience.

[33]  H. Critchley,et al.  The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. , 2000, Brain : a journal of neurology.

[34]  C. Keysers,et al.  A Common Anterior Insula Representation of Disgust Observation, Experience and Imagination Shows Divergent Functional Connectivity Pathways , 2008, PloS one.

[35]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[36]  S. Delplanque,et al.  Beyond Conventional Event-related Brain Potential (ERP): Exploring the Time-course of Visual Emotion Processing Using Topographic and Principal Component Analyses , 2008, Brain Topography.

[37]  Dimitri Van De Ville,et al.  Decoding of Emotional Information in Voice-Sensitive Cortices , 2009, Current Biology.

[38]  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.

[39]  R. Hari,et al.  Emotions promote social interaction by synchronizing brain activity across individuals , 2012, Proceedings of the National Academy of Sciences.

[40]  Dimitri Van De Ville,et al.  Impact of transient emotions on functional connectivity during subsequent resting state: A wavelet correlation approach , 2011, NeuroImage.

[41]  Katherine Vytal,et al.  Neuroimaging Support for Discrete Neural Correlates of Basic Emotions: A Voxel-based Meta-analysis , 2010, Journal of Cognitive Neuroscience.

[42]  K. Scherer,et al.  Appraisal processes in emotion. , 2003 .

[43]  Tom Michael Mitchell,et al.  Predicting Human Brain Activity Associated with the Meanings of Nouns , 2008, Science.

[44]  C. Izard,et al.  Four systems for emotion activation: cognitive and noncognitive processes. , 1993, Psychological review.

[45]  Joseph E LeDoux Rethinking the Emotional Brain , 2012, Neuron.

[46]  E. Rolls Emotion and decision making explained , 2013 .

[47]  Kalanit Grill-Spector,et al.  Sparsely-distributed organization of face and limb activations in human ventral temporal cortex , 2010, NeuroImage.

[48]  D. Tilman,et al.  Plant species loss decreases arthropod diversity and shifts trophic structure. , 2009, Ecology letters.

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

[50]  G. Essick,et al.  Touching and feeling: differences in pleasant touch processing between glabrous and hairy skin in humans , 2012, The European journal of neuroscience.

[51]  L. F. Barrett Discrete Emotions or Dimensions? The Role of Valence Focus and Arousal Focus , 1998 .

[52]  Ivanei E. Bramati,et al.  The Moral Affiliations of Disgust: A Functional MRI Study , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[53]  B. King-Casas,et al.  The neurobiology of social decision-making , 2008, Current Opinion in Neurobiology.

[54]  R. Schultz,et al.  The perception and identification of facial emotions in individuals with autism spectrum disorders using the Let's Face It! Emotion Skills Battery. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[55]  E. Rolls,et al.  Cognitive Modulation of Olfactory Processing , 2005, Neuron.

[56]  P. Ekman,et al.  What is Meant by Calling Emotions Basic , 2011 .

[57]  H Scheich,et al.  Auditory perception of laughing and crying activates human amygdala regardless of attentional state. , 2001, Brain research. Cognitive brain research.

[58]  S. Roux,et al.  Early visual ERPs are influenced by individual emotional skills. , 2014, Social cognitive and affective neuroscience.

[59]  J. Grèzes,et al.  Emotional modulation of visual and motor areas by dynamic body expressions of anger , 2008, Social neuroscience.

[60]  Jan Schweckendiek,et al.  Contingency learning in human fear conditioning involves the ventral striatum , 2009, Human brain mapping.

[61]  R. Stark,et al.  The insula is not specifically involved in disgust processing: an fMRI study , 2002, Neuroreport.

[62]  Tommaso Costa,et al.  Distinct pathways of neural coupling for different basic emotions , 2012, NeuroImage.

[63]  Cristina Ramponi,et al.  The amygdala response to images with impact. , 2009, Social cognitive and affective neuroscience.

[64]  Jennifer C. Britton,et al.  Neural correlates of social and nonsocial emotions: An fMRI study , 2006, NeuroImage.

[65]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

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

[67]  J. Panksepp,et al.  What is Basic about Basic Emotions? Lasting Lessons from Affective Neuroscience , 2011 .

[68]  Alexander Todorov,et al.  Brain systems for assessing the affective value of faces , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[70]  L. F. Barrett Solving the Emotion Paradox: Categorization and the Experience of Emotion , 2006, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[71]  R. Zatorre,et al.  Anatomically distinct dopamine release during anticipation and experience of peak emotion to music , 2011, Nature Neuroscience.

[72]  A. Lawrence,et al.  Appetitive Motivation Predicts the Neural Response to Facial Signals of Aggression , 2008, The Journal of Neuroscience.

[73]  L. Pessoa,et al.  Positive emotions broaden the scope of attention and thought‐action repertoires , 2005, Cognition & emotion.

[74]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[75]  P. Ekman Universals and cultural differences in facial expressions of emotion. , 1972 .

[76]  R. Khan,et al.  Predicting Odor Pleasantness from Odorant Structure: Pleasantness as a Reflection of the Physical World , 2007, The Journal of Neuroscience.

[77]  T. Kircher,et al.  Supramodal Representation of Emotions , 2011, The Journal of Neuroscience.

[78]  L. Pessoa On the relationship between emotion and cognition , 2008, Nature Reviews Neuroscience.

[79]  Frank Schneider,et al.  Real-time fMRI of temporolimbic regions detects amygdala activation during single-trial self-induced sadness , 2003, NeuroImage.

[80]  Lars Muckli,et al.  Classification images reveal the information sensitivity of brain voxels in fMRI , 2008, NeuroImage.

[81]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[82]  R. Dolan,et al.  The Nose Smells What the Eye Sees Crossmodal Visual Facilitation of Human Olfactory Perception , 2003, Neuron.

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

[84]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

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

[86]  Talma Hendler,et al.  Feeling the real world: limbic response to music depends on related content. , 2007, Cerebral cortex.

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

[88]  Michèle Wessa,et al.  An Agent Harms a Victim: A Functional Magnetic Resonance Imaging Study on Specific Moral Emotions , 2008, Journal of Cognitive Neuroscience.

[89]  R. Dolan,et al.  Crossmodal binding of fear in voice and face , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[90]  A. Damasio,et al.  Persistence of feelings and sentience after bilateral damage of the insula. , 2013, Cerebral cortex.

[91]  S. Koelsch Towards a neural basis of music-evoked emotions , 2010, Trends in Cognitive Sciences.

[92]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[93]  M. Bradley,et al.  Emotion and the motivational brain , 2010, Biological Psychology.

[94]  U. Wagner,et al.  Guilt-specific processing in the prefrontal cortex. , 2011, Cerebral cortex.

[95]  Philip A. Gable,et al.  The motivational dimensional model of affect: Implications for breadth of attention, memory, and cognitive categorisation , 2010 .

[96]  Wolfgang Grodd,et al.  Differential Influences of Emotion, Task, and Novelty on Brain Regions Underlying the Processing of Speech Melody , 2009, Journal of Cognitive Neuroscience.

[97]  Talma Hendler,et al.  Eyes Wide Shut: Amygdala Mediates Eyes-Closed Effect on Emotional Experience with Music , 2009, PloS one.

[98]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[99]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

[100]  Didier Grandjean,et al.  Multiple subregions in superior temporal cortex are differentially sensitive to vocal expressions: A quantitative meta-analysis , 2013, Neuroscience & Biobehavioral Reviews.

[101]  A. Jacobs,et al.  How music alters a kiss: superior temporal gyrus controls fusiform-amygdalar effective connectivity. , 2014, Social cognitive and affective neuroscience.

[102]  M. Delgado,et al.  Reward‐Related Responses in the Human Striatum , 2007, Annals of the New York Academy of Sciences.

[103]  C. Izard Forms and Functions of Emotions: Matters of Emotion–Cognition Interactions , 2011 .

[104]  Lisa Feldman Barrett,et al.  Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies , 2008, NeuroImage.

[105]  Yoshiro Okubo,et al.  Brain activations during judgments of positive self-conscious emotion and positive basic emotion: pride and joy. , 2008, Cerebral cortex.

[106]  U. Eysel,et al.  Neural structures associated with recognition of facial expressions of basic emotions , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[107]  M. Peelen,et al.  Supramodal Representations of Perceived Emotions in the Human Brain , 2010, The Journal of Neuroscience.

[108]  Patrik Vuilleumier,et al.  Individual Attachment Style Modulates Human Amygdala and Striatum Activation during Social Appraisal , 2008, PloS one.

[109]  R. Post,et al.  Regional brain activity during transient self-induced anxiety and anger in healthy adults , 1999, Biological Psychiatry.

[110]  M. Zentner,et al.  Mapping Aesthetic Musical Emotions in the Brain , 2011, Cerebral cortex.

[111]  Ewald Moser,et al.  General and specific responsiveness of the amygdala during explicit emotion recognition in females and males , 2009, BMC Neuroscience.

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

[113]  Jong-Min Lee,et al.  Integration of cross-modal emotional information in the human brain: An fMRI study , 2010, Cortex.

[114]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[115]  Nathalie George,et al.  The Cambridge Handbook of Human Affective Neuroscience: The Facial Expression of Emotions , 2013 .

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

[117]  Paul Cumming,et al.  Dopamine in amygdala gates limbic processing of aversive stimuli in humans , 2008, Nature Neuroscience.

[118]  Arne Öhman,et al.  Phobias and preparedness: the selective, automatic, and encapsulated nature of fear , 2002, Biological Psychiatry.

[119]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

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

[121]  N. Sadato,et al.  Age‐related differences in the medial temporal lobe responses to emotional faces as revealed by fMRI , 2002, Hippocampus.

[122]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[123]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[124]  A. Craig A new view of pain as a homeostatic emotion , 2003, Trends in Neurosciences.

[125]  Patrik Vuilleumier,et al.  Emotional modulation of body-selective visual areas. , 2007, Social cognitive and affective neuroscience.

[126]  Markus Junghöfer,et al.  Neuroimaging methods in affective neuroscience: selected methodological issues. , 2006, Progress in brain research.

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

[128]  Michael J. Brammer,et al.  A preferential increase in the extrastriate response to signals of danger , 2003, NeuroImage.

[129]  Charles D. Smith,et al.  Neural substrates of facial emotion processing using fMRI. , 2001, Brain research. Cognitive brain research.

[130]  Jörg Bahlmann,et al.  Predicting vocal emotion expressions from the human brain , 2013, Human brain mapping.

[131]  Patrik Vuilleumier,et al.  Self-relevance processing in the human amygdala: gaze direction, facial expression, and emotion intensity. , 2009, Emotion.

[132]  I. Peretz,et al.  Impaired recognition of musical emotions and facial expressions following anteromedial temporal lobe excision , 2011, Cortex.

[133]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[134]  Julien Cohen-Adad,et al.  Identification of discrete functional subregions of the human periaqueductal gray , 2013, Proceedings of the National Academy of Sciences.

[135]  Jill Keane,et al.  Impaired recognition of anger following damage to the ventral striatum. , 2004, Brain : a journal of neurology.

[136]  Jeesun Kim,et al.  Emotional expressions evoke a differential response in the fusiform face area , 2013, Front. Hum. Neurosci..

[137]  Matthew Brett,et al.  Rhythm and Beat Perception in Motor Areas of the Brain , 2007, Journal of Cognitive Neuroscience.

[138]  Matthew D. Lieberman,et al.  Social cognitive neuroscience: a review of core processes. , 2007, Annual review of psychology.

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

[140]  P. Griffiths,et al.  Don’t Give Up on Basic Emotions , 2011 .

[141]  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.

[142]  Lutz Jäncke,et al.  The emotional power of music: How music enhances the feeling of affective pictures , 2006, Brain Research.

[143]  Paul Pavlidis,et al.  Decoding Unattended Fearful Faces with Whole-Brain Correlations: An Approach to Identify Condition-Dependent Large-Scale Functional Connectivity , 2012, PLoS Comput. Biol..

[144]  Luca Passamonti,et al.  Abnormal Anatomical Connectivity between the Amygdala and Orbitofrontal Cortex in Conduct Disorder , 2012, PloS one.

[145]  Martial Van der Linden,et al.  Neural correlates of “hot” and “cold” emotional processing: a multilevel approach to the functional anatomy of emotion , 2003, NeuroImage.

[146]  Pascal Belin,et al.  Amygdala responses to nonlinguistic emotional vocalizations , 2007, NeuroImage.

[147]  D. Wildgruber,et al.  Emotional voice areas: anatomic location, functional properties, and structural connections revealed by combined fMRI/DTI. , 2012, Cerebral cortex.

[148]  C. Darwin The Expression of the Emotions in Man and Animals , .

[149]  Clement Hamani,et al.  Neuronal Coding of Implicit Emotion Categories in the Subcallosal Cortex in Patients with Depression , 2013, Biological Psychiatry.

[150]  R. Elliott,et al.  The neural response to emotional prosody, as revealed by functional magnetic resonance imaging , 2003, Neuropsychologia.

[151]  Joseph J Paton,et al.  Flexible Neural Representations of Value in the Primate Brain , 2007, Annals of the New York Academy of Sciences.

[152]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[153]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[154]  J. O'Doherty,et al.  Regret and its avoidance: a neuroimaging study of choice behavior , 2005, Nature Neuroscience.

[155]  A. Hammers,et al.  Evidence for endogenous opioid release in the amygdala during positive emotion , 2009, NeuroImage.

[156]  Wolfgang Grodd,et al.  It is not always tickling: Distinct cerebral responses during perception of different laughter types , 2010, NeuroImage.

[157]  Christoph M. Michel,et al.  Early neuronal responses in right limbic structures mediate harmony incongruity processing in musical experts , 2008, NeuroImage.

[158]  Patrik Vuilleumier,et al.  Processing social aspects of human gaze: A combined fMRI-DTI study , 2011, NeuroImage.

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

[160]  K. Scherer,et al.  The voices of wrath: brain responses to angry prosody in meaningless speech , 2005, Nature Neuroscience.

[161]  A. Young,et al.  Configural information in facial expression perception. , 2000, Journal of experimental psychology. Human perception and performance.

[162]  S. Koelsch,et al.  Tension-related activity in the orbitofrontal cortex and amygdala: an fMRI study with music. , 2014, Social cognitive and affective neuroscience.

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

[164]  K. Scherer,et al.  The World of Emotions is not Two-Dimensional , 2007, Psychological science.

[165]  J. Wessberg,et al.  Coding of pleasant touch by unmyelinated afferents in humans , 2009, Nature Neuroscience.

[166]  Dimitri Van De Ville,et al.  Decoding brain states from fMRI connectivity graphs , 2011, NeuroImage.

[167]  François Mauguière,et al.  Experiencing and detecting happiness in humans: The role of the supplementary motor area , 2006, Annals of neurology.