A common neural basis for receptive and expressive communication of pleasant facial affect

There is accumulating evidence suggesting that the visual representation of facial affect is closely linked to its motor representation. To examine whether perception of pleasant facial affect involves neural circuitries associated with its production, we performed an fMRI experiment with 'compressed image acquisition' where subjects smiled and observed movies depicting other people smiling within scan-free time intervals between the acquisition of each image volume. Overlaps between the brain activation during observation and execution of smile expressions were located in the right premotor cortex and pars opercularis of the inferior frontal gyrus, right parietal operculum (SII) and left anterior insula. Observation of smile expressions further yielded signal increases within the posterior superior temporal sulcus (STS), fusiform gyrus and ventral amygdala. The results show that perceiving and expressing pleasant facial affect share a common neural basis in areas concerned with motor as well as somato- and limbic-sensory processing. In concert with temporal regions serving the visual analysis of facial expressive features, a mapping of the observed expressions onto neural circuitries associated with the production of these expressions and its somatosensory consequences could provide a description of what the expression would feel like if produced in the observer. Such a mechanism is suggested to be important for empathic understanding of others' feelings.

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

[2]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[3]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[4]  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.

[5]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[6]  A. Giannini,et al.  Defective response to social cues in Möbius' syndrome. , 1984, The Journal of nervous and mental disease.

[7]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

[8]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[9]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

[10]  R W Cox,et al.  Magnetic field changes in the human brain due to swallowing or speaking , 1998, Magnetic resonance in medicine.

[11]  R. Adolphs Recognizing emotion from facial expressions: psychological and neurological mechanisms. , 2002, Behavioral and cognitive neuroscience reviews.

[12]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[13]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[14]  B. Kapp,et al.  Neuronal activity within the nucleus basalis and conditioned neocortical electroencephalographic activation , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[16]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Damasio Descartes’ Error. Emotion, Reason and the Human Brain. New York (Grosset/Putnam) 1994. , 1994 .

[18]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

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

[20]  H. E. Brown,et al.  Utilizing hemodynamic delay and dispersion to detect fMRI signal change without auditory interference: The behavior interleaved gradients technique , 1999, Magnetic resonance in medicine.

[21]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[23]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[24]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[25]  E C Wong,et al.  Effect of motion outside the field of view on functional MR. , 1996, AJNR. American journal of neuroradiology.

[26]  R. Hari,et al.  Modulated Activation of the Human SI and SII Cortices during Observation of Hand Actions , 2002, NeuroImage.

[27]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[28]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

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

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

[31]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[33]  R. J. Seitz,et al.  A fronto‐parietal circuit for object manipulation in man: evidence from an fMRI‐study , 1999, The European journal of neuroscience.

[34]  J V Hajnal,et al.  Stimulus-correlated signals in functional MR of the brain. , 1996, AJNR. American journal of neuroradiology.

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

[36]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[37]  R. Bowtell,et al.  “sparse” temporal sampling in auditory fMRI , 1999, Human brain mapping.

[38]  R W Cox,et al.  Event‐related fMRI of tasks involving brief motion , 1999, Human brain mapping.

[39]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[40]  A Weindl,et al.  Neural correlates associated with impaired disgust processing in pre-symptomatic Huntington's disease. , 2004, Brain : a journal of neurology.

[41]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[42]  G. Rizzolatti,et al.  ß Federation of European Neuroscience Societies Mirror , 2003 .

[43]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[44]  Michael Erb,et al.  Why are smiles contagious? An fMRI study of the interaction between perception of facial affect and facial movements , 2003, Psychiatry Research: Neuroimaging.

[45]  Steve C R Williams,et al.  Acoustic noise and functional magnetic resonance imaging: Current strategies and future prospects , 2002, Journal of magnetic resonance imaging : JMRI.

[46]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[47]  Judee K. Burgoon,et al.  Reacting to nonverbal expressions of liking: A test of interaction adaptation theory , 1999 .

[48]  H. Critchley,et al.  Neuroanatomical basis for first- and second-order representations of bodily states , 2001, Nature Neuroscience.

[49]  J. Hyde,et al.  Localization of the Cortical Response to Smiling Using New Imaging Paradigms with Functional Magnetic Resonance Imaging , 2001, Plastic and reconstructive surgery.

[50]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[51]  A. Goldman,et al.  Simulationist models of face-based emotion recognition , 2005, Cognition.

[52]  N. A. Borghese,et al.  Different Brain Correlates for Watching Real and Virtual Hand Actions , 2001, NeuroImage.

[53]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[54]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[55]  M. Iacoboni Understanding Others: Imitation, Language, Empathy , 2002 .

[56]  R. Weisskoff,et al.  Improved auditory cortex imaging using clustered volume acquisitions , 1999, Human brain mapping.

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

[58]  Andrew L. Alexander,et al.  uman Amygdala Responses During Presentation of appy and Neutral Faces : Correlations with State nxiety eah , 2004 .

[59]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[60]  Scott T Grafton,et al.  Functional imaging of face and hand imitation: towards a motor theory of empathy , 2004, NeuroImage.

[61]  J. Decety,et al.  Top down effect of strategy on the perception of human biological motion: a pet investigation. , 1998, Cognitive neuropsychology.

[62]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[63]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[64]  R. Zajonc,et al.  Facial efference and the experience of emotion. , 1989, Annual review of psychology.

[65]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[66]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[67]  R. J. Dolan,et al.  Functional Magnetic Resonance Imaging of Proactive Interference during Spoken Cued Recall , 2002, NeuroImage.

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

[69]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[70]  P. Ekman,et al.  Voluntary facial action generates emotion-specific autonomic nervous system activity. , 1990, Psychophysiology.

[71]  U. Dimberg,et al.  Facial reactions to happy and angry facial expressions: evidence for right hemisphere dominance. , 2000, Psychophysiology.

[72]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[73]  H. Critchley,et al.  Fear Conditioning in Humans The Influence of Awareness and Autonomic Arousal on Functional Neuroanatomy , 2002, Neuron.

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

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

[76]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[77]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[78]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

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

[80]  A. Young,et al.  FACIAL EXPRESSION RECOGNITION BY PEOPLE WITH MÖBIUS SYNDROME , 2000, Cognitive neuropsychology.

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