Neural Substrates of Human Facial Expression of Pleasant Emotion Induced by Comic Films: A PET Study

Laughter or smile is one of the emotional expressions of pleasantness with characteristic contraction of the facial muscles, of which the neural substrate remains to be explored. This currently described study is the first to investigate the generation of human facial expression of pleasant emotion using positron emission tomography and H(2)(15)O. Regional cerebral blood flow (rCBF) during laughter/smile induced by visual comics and the magnitude of laughter/smile indicated significant correlation in the bilateral supplementary motor area (SMA) and left putamen (P < 0.05, corrected), but no correlation in the primary motor area (M1). In the voluntary facial movement, significant correlation between rCBF and the magnitude of EMG was found in the face area of bilateral M1 and the SMA (P < 0.001, uncorrected). Laughter/smile, as opposed to voluntary movement, activated the visual association areas, left anterior temporal cortex, left uncus, and orbitofrontal and medial prefrontal cortices (P < 0.05, corrected), whereas voluntary facial movement generated by mimicking a laughing/smiling face activated the face area of the left M1 and bilateral SMA, compared with laughter/smile (P < 0.05, corrected). We demonstrated distinct neural substrates of emotional and volitional facial expression and defined cognitive and experiential processes of a pleasant emotion, laughter/smile.

[1]  R. Ross,et al.  Volitional and Emotional Supranuclear Facial Weakness , 1998 .

[2]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[3]  S. Paradiso,et al.  Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. , 1999, The American journal of psychiatry.

[4]  C. Fitzek,et al.  Isolated voluntary facial paresis due to pontine ischemia , 1998, Neurology.

[5]  A. J. Fridlund,et al.  Guidelines for human electromyographic research. , 1986, Psychophysiology.

[6]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[7]  L. Jäncke,et al.  Tapping movements according to regular and irregular visual timing signals investigated with fMRI , 2000, Neuroreport.

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

[9]  M. Mendez,et al.  Involuntary laughter and inappropriate hilarity. , 1999, The Journal of neuropsychiatry and clinical neurosciences.

[10]  G. Boulogne,et al.  The Mechanism of Human Facial Expression , 1990 .

[11]  C. Fitzek,et al.  Emotional facial paresis of pontine origin , 2000, Neurology.

[12]  L. Baden,et al.  "Images in clinical medicine". , 2001, Connecticut medicine.

[13]  H Shibasaki,et al.  The functions of the supplementary motor area. Summary of a workshop. , 1996, Advances in neurology.

[14]  L. Rubin The Mechanism of Human Facial Expression , 1992 .

[15]  James L. Herrick,et al.  Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression. , 2001, Brain : a journal of neurology.

[16]  A R Damasio,et al.  Pathological laughter and crying: a link to the cerebellum. , 2001, Brain : a journal of neurology.

[17]  S. G. Cox,et al.  Functional MRI study of the cognitive generation of affect. , 1999, The American journal of psychiatry.

[18]  G. Klerman,et al.  Facial Expression and Imagery in Depression: An Electromyographic Study , 1976, Psychosomatic medicine.

[19]  Hans Kruuk,et al.  Non-verbal Communication , 1973 .

[20]  P. Ekman,et al.  The Duchenne smile: emotional expression and brain physiology. II. , 1990, Journal of personality and social psychology.

[21]  Richard S. J. Frackowiak,et al.  Detection of Thirty-Second Cognitive Activations in Single Subjects with Positron Emission Tomography: A New Low-Dose H215O Regional Cerebral Blood Flow Three-Dimensional Imaging Technique , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  P. Hansotia,et al.  Gelastic epilepsy. , 1970, British medical journal.

[23]  R. Hassler,et al.  [Effects of stimulations and coagulations in the basal ganglia in stereotactic brain surgery]. , 1961, Der Nervenarzt.

[24]  P. Loiseau,et al.  Gelastic Epilepsy A Review and Report of Five Cases , 1971, Epilepsia.

[25]  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 .

[26]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[27]  R. Dolan,et al.  The functional anatomy of humor: segregating cognitive and affective components , 2001, Nature Neuroscience.

[28]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[29]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[30]  R. Ross,et al.  Images in clinical medicine. Volitional and emotional supranuclear facial weakness. , 1998, The New England journal of medicine.

[31]  H Okada,et al.  Brain activation during maintenance of standing postures in humans. , 1999, Brain : a journal of neurology.

[32]  V. Hooff A comparative approach to the phylogeny of laughter and smiling. , 1972 .

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

[34]  H. Hopf,et al.  Localization of emotional and volitional facial paresis , 1992, Neurology.

[35]  R. Töpper,et al.  Volitional type of facial palsy associated with pontine ischaemia. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[36]  J. Talairach,et al.  Clinical consequences of corticectomies involving the supplementary motor area in man , 1977, Journal of the Neurological Sciences.

[37]  K Shinosaki,et al.  Diminished facial expression despite the existence of pleasant emotional experience in schizophrenia. , 1999, Methods and findings in experimental and clinical pharmacology.

[38]  P P Urban,et al.  The course of corticofacial projections in the human brainstem. , 2001, Brain : a journal of neurology.

[39]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[40]  R P Lesser,et al.  Mirth, laughter and gelastic seizures. , 1993, Brain : a journal of neurology.

[41]  G. Gascon,et al.  Epileptic (Gelastic) Laughter , 1971, Epilepsia.

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

[43]  J. Dichgans,et al.  Voluntary facial palsy with a pontine lesion. , 1996, Journal of neurology, neurosurgery, and psychiatry.