Gender differences in the neural network of facial mimicry of smiles - An rTMS study

Cortex

Volumn 70, Issue , 2015, Pages 101-114

  Korb, Sebastian ^a   Malsert, Jennifer ^b   Rochas, Vincent ^b   Rihs, Tonia A ^b   Rieger, Sebastian W ^b   Schwab, Samir ^b   Niedenthal, Paula M ^c   Grandjean, Didier ^b  

^a SISSA   (Italy)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Facial mimicry; Gender differences; Motor cortex; Somatosensory cortex; TMS

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; EMOTION; FACIAL EXPRESSION; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; MIRROR NEURON; NERVE CELL NETWORK; NORMAL HUMAN; PERCEPTION; PRIMARY MOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; QUESTIONNAIRE; RESPONSE TIME; SEX DIFFERENCE; TRANSCRANIAL MAGNETIC STIMULATION; FACIAL RECOGNITION; IMITATION; MOTOR CORTEX; NERVE TRACT; PHYSIOLOGY; SOMATOSENSORY CORTEX; YOUNG ADULT;

ADULT; FACIAL EXPRESSION; FACIAL RECOGNITION; FEMALE; HUMANS; IMITATIVE BEHAVIOR; MALE; MOTOR CORTEX; NEURAL PATHWAYS; SEX FACTORS; SMILING; SOCIAL PERCEPTION; SOMATOSENSORY CORTEX; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84939560050     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2015.06.025     Document Type: Article

References (70)

1. Achaibou A., Pourtois G., Schwartz S., Vuilleumier P. Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry. Neuropsychologia 2008, 46(4):1104-1113. 10.1016/j.neuropsychologia.2007.10.019.
2. Adelmann P.K., Zajonc R.B. Facial efference and the experience of emotion. Annual Review of Psychology 1989, 40(1):249-280. 10.1146/annurev.ps.40.020189.001341.
3. Adolphs R., Damasio H., Tranel D., Cooper G., Damasio A.R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. Journal of Neuroscience 2000, 20(7):2683-2690.
4. Balconi M., Bortolotti A. Conscious and unconscious face recognition is improved by high-frequency rTMS on pre-motor cortex. Consciousness and Cognition 2013, 22(3):771-778. 10.1016/j.concog.2013.04.013.
5. Balconi M., Bortolotti A. The "simulation" of the facial expression of emotions in case of short and long stimulus duration. The effect of pre-motor cortex inhibition by rTMS. Brain and Cognition 2013, 83(1):114-120. 10.1016/j.bandc.2013.07.003.
6. Balconi M., Canavesio Y. High-frequency rTMS improves facial mimicry and detection responses in an empathic emotional task. Neuroscience 2013, 236:12-20. 10.1016/j.neuroscience.2012.12.059.
7. Baron-Cohen S., Wheelwright S. The empathy quotient: an investigation of adults with asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders 2004, 34(2):163-175.
8. Barsalou L.W. Grounded cognition. Annual Review of Psychology 2008, 59(1):617-645.
9. Buck R. Nonverbal behavior and the theory of emotion: the facial feedback hypothesis. Journal of Personality and Social Psychology 1980, 38(5):811-824. 10.1037/0022-3514.38.5.811.
10. Cahill L. A half-truth is a whole lie: on the necessity of investigating sex influences on the brain. Endocrinology 2012, 153(6):2541-2543. 10.1210/en.2011-2167.
11. Darwin C. The expression of the emotions in man and animals 1872, John Murray, UK.
12. Davis M.H. Measuring individual differences in empathy: evidence for a multidimensional approach. Journal of Personality and Social Psychology 1983, 44(1):113-126. 10.1037/0022-3514.44.1.113.
13. De Wied M., van Boxtel A., Zaalberg R., Goudena P.P., Matthys W. Facial EMG responses to dynamic emotional facial expressions in boys with disruptive behavior disorders. Journal of Psychiatric Research 2006, 40(2):112-121. (PII: S0022-3956(05)00099-3). 10.1016/j.jpsychires.2005.08.003.
14. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods 2004, 134(1):9-21. 10.1016/j.jneumeth.2003.10.009.
15. Di Pellegrino G., Fadiga L., Fogassi L., Gallese V., Rizzolatti G. Understanding motor events: a neurophysiological study. Experimental Brain Research 1992, 91(1):176-180.
16. Dimberg U., Andréasson P., Thunberg M. Emotional empathy and facial reactions to facial expressions. Journal of Psychophysiology 2011, 25(1):26-31. 10.1027/0269-8803/a000029.
17. Dimberg U., Lundquist L.O. Gender differences in facial reactions to facial expressions. Biological Psychology 1990, 30(2):151-159.
18. Dimberg U., Thunberg M., Elmehed K. Unconscious facial reactions to emotional facial expressions. Psychological Science 2000, 11(1):86-89.
19. Dimberg U., Thunberg M., Grunedal S. Facial reactions to emotional stimuli: automatically controlled emotional responses. Cognition and Emotion 2002, 16(4):449-472.
20. Doherty R.W., Orimoto L., Singelis T.M., Hatfield E., Hebb J. Emotional contagion: gender and occupational differences. Psychology of Women Quarterly 1995, 19(3):355-371. 10.1111/j.1471-6402.1995.tb00080.x.
21. Eisenberg N., Lennon R. Sex differences in empathy and related capacities. Psychological Bulletin 1983, 94(1):100-131.
22. Ekman P., Levenson R.W., Friesen W.V. Autonomic nervous system activity distinguishes among emotions. Science 1983, 221(4616):1208-1210.
23. Finzi E., Rosenthal N.E. Treatment of depression with onabotulinumtoxinA: a randomized, double-blind, placebo controlled trial. Journal of Psychiatric Research 2014, 52:1-6. 10.1016/j.jpsychires.2013.11.006.
24. Fridlund A.J., Cacioppo J.T. Guidelines for human electromyographic research. Psychophysiology 1986, 23(5):567-589. 10.1111/j.1469-8986.1986.tb00676.x.
25. Gazzola V., Keysers C. The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cerebral Cortex (New York, N.Y.: 1991) 2009, 19(6):1239-1255.
26. Goldsworthy M.R., Pitcher J.B., Ridding M.C. A comparison of two different continuous theta burst stimulation paradigms applied to the human primary motor cortex. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 2012, 123(11):2256-2263. 10.1016/j.clinph.2012.05.001.
27. Halberstadt J., Niedenthal P.M. Effects of emotion concepts on perceptual memory for emotional expressions. Journal of Personality and Social Psychology 2001, 81(4):587-598. 10.1037//0022-3514.81.4.587.
28. Hall J.A. Gender effects in decoding nonverbal cues. Psychological Bulletin 1978, 85(4):845-857. 10.1037/0033-2909.85.4.845.
29. Hall J.A., Matsumoto D. Gender differences in judgments of multiple emotions from facial expressions. Emotion (Washington, D.C.) 2004, 4(2):201-206. 10.1037/1528-3542.4.2.201.
30. Hatfield E., Cacioppo J.T., Rapson R.L. Emotional contagion. Current Directions in Psychological Science 1993, 2(3):96-100. 10.1111/1467-8721.ep10770953.
31. Hennenlotter A., Dresel C., Castrop F., Ceballos-Baumann A.O., Baumann A.O.C., Wohlschläger A.M., et al. The link between facial feedback and neural activity within central circuitries of emotion-new insights from botulinum toxin-induced denervation of frown muscles. Cerebral Cortex 2009, 19(3):537-542. 10.1093/cercor/bhn104.
32. Hess U., Blairy S. Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy. International Journal of Psychophysiology 2001, 40(2):129-141.
33. Hoffmann H., Kessler H., Eppel T., Rukavina S., Traue H.C. Expression intensity, gender and facial emotion recognition: women recognize only subtle facial emotions better than men. Acta Psychologica 2010, 135(3):278-283. 10.1016/j.actpsy.2010.07.012.
34. Iacoboni M. Imitation, empathy, and mirror neurons. Annual Review of Psychology 2009, 60:653-670. 10.1146/annurev.psych.60.110707.163604.
35. James W. The principles of psychology 1950, Dover, New York.
36. Keysers C., Kaas J.H., Gazzola V. Somatosensation in social perception. Nature Reviews Neuroscience 2010, 11(6):417-428. 10.1038/nrn2833.
37. Korb S., Grandjean D., Scherer K.R. Timing and voluntary suppression of facial mimicry to smiling faces in a Go/NoGo task-an EMG study. Biological Psychology 2010, 85(2):347-349. 10.1016/j.biopsycho.2010.07.012.
38. Korb S., With S., Niedenthal P.M., Kaiser S., Grandjean D. The perception and mimicry of facial movements predict judgments of smile authenticity. PLoS One 2014, 9(6):e99194. 10.1371/journal.pone.0099194.
39. Kring A.M., Gordon A.H. Sex differences in emotion: expression, experience, and physiology. Journal of Personality and Social Psychology 1998, 74(3):686-703.
40. Likowski K.U., Mühlberger A., Gerdes A.B.M., Wieser M.J., Pauli P., Weyers P. Facial mimicry and the mirror neuron system: simultaneous acquisition of facial electromyography and functional magnetic resonance imaging. Frontiers in Human Neuroscience 2012, 6(214). 10.3389/fnhum.2012.00214.
41. Lipps T. Einfühlung, innere Nachahmung, und Organempfindungen. Archiv Für Die Gesamte Psychologie 1903, 1:185-204.
42. Maringer M., Krumhuber E.G., Fischer A.H., Niedenthal P.M. Beyond smile dynamics: mimicry and beliefs in judgments of smiles. Emotion (Washington, D.C.) 2011, 11(1):181-187. 10.1037/a0022596.
43. Mathersul D., McDonald S., Rushby J.A. Automatic facial responses to briefly presented emotional stimuli in autism spectrum disorder. Biological Psychology 2013, 10.1016/j.biopsycho.2013.08.004.
44. McIntosh D.N. Facial feedback hypotheses: evidence, implications, and directions. Motivation and Emotion 1996, 20(2):121-147. 10.1007/BF02253868.
45. Molenberghs P., Cunnington R., Mattingley J.B. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neuroscience and Biobehavioral Reviews 2012, 36(1):341-349. 10.1016/j.neubiorev.2011.07.004.
46. Moody E.J., McIntosh D.N., Mann L.J., Weisser K.R. More than mere mimicry? The influence of emotion on rapid facial reactions to faces. Emotion (Washington, D.C.) 2007, 7(2):447-457.
47. Mukamel R., Ekstrom A.D., Kaplan J., Iacoboni M., Fried I. Single-neuron responses in humans during execution and observation of actions. Current Biology 2010, 20(8):750-756. 10.1016/j.cub.2010.02.045.
48. Niedenthal P.M. Embodying emotion. Science 2007, 316(5827):1002-1005.
49. Niedenthal P.M., Augustinova M., Rychlowska M., Droit-Volet S., Zinner L., Knafo A., et al. Negative relations between pacifier use and emotional competence. Basic and Applied Social Psychology 2012, 34(5):387-394. 10.1080/01973533.2012.712019.
50. Niedenthal P.M., Brauer M., Halberstadt J.B., Innes-Ker Å.H. When did her smile drop? Facial mimicry and the influences of emotional state on the detection of change in emotional expression. Cognition and Emotion 2001, 15(16):853-864.
51. Nyffeler T., Wurtz P., Lüscher H.-R., Hess C.W., Senn W., Pflugshaupt T., et al. Repetitive TMS over the human oculomotor cortex: comparison of 1-Hz and theta burst stimulation. Neuroscience Letters 2006, 409(1):57-60. 10.1016/j.neulet.2006.09.011.
52. Oberman L.M., Winkielman P., Ramachandran V.S. Face to face: blocking facial mimicry can selectively impair recognition of emotional expressions. Social Neuroscience 2007, 2(3-4):167-178.
53. Pitcher D., Garrido L., Walsh V., Duchaine B.C. Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. Journal of Neuroscience 2008, 28(36):8929-8933.
54. Pourtois G., Sander D., Andres M., Grandjean D., Reveret L., Olivier E., et al. Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. European Journal of Neuroscience 2004, 20(12):3507-3515.
55. Rieger S.W., Domínguez-Borràs J., Vuilleumier P. An MRI compatible somatosensory stimulation device for the investigation of crossmodal effects of emotion on the processing of tactile, visual, and auditory input 2011, Presented at the ESMRMB Annual Meeting, Leipzig.
56. Rives Bogart K., Matsumoto D. Facial mimicry is not necessary to recognize emotion: facial expression recognition by people with Moebius syndrome. Social Neuroscience 2010, 5(2):241. 10.1080/17470910903395692.
57. Rizzolatti G., Craighero L. The mirror-neuron system. Annual Review of Neuroscience 2004, 27:169-192. 10.1146/annurev.neuro.27.070203.144230.
58. Rizzolatti G., Fogassi L., Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience 2001, 2(9):661-670.
59. Rochas V., Gelmini L., Krolak-Salmon P., Poulet E., Saoud M., Brunelin J., et al. Disrupting pre-SMA activity impairs facial happiness recognition: an event-related TMS study. Cerebral Cortex (New York, N.Y.: 1991) 2013, 23(7):1517-1525. 10.1093/cercor/bhs133.
60. Rychlowska M., Cañadas E., Wood A., Krumhuber E.G., Fischer A., Niedenthal P.M. Blocking mimicry makes true and false smiles look the same. PLoS One 2014, 9(3):e90876. 10.1371/journal.pone.0090876.
61. Schilbach L., Eickhoff S.B., Mojzisch A., Vogeley K. What's in a smile? Neural correlates of facial embodiment during social interaction. Social Neuroscience 2008, 3(1):37-50.
62. Sims T.B., Van Reekum C.M., Johnstone T., Chakrabarti B. How reward modulates mimicry: EMG evidence of greater facial mimicry of more rewarding happy faces. Psychophysiology 2012, 49(7):998-1004. 10.1111/j.1469-8986.2012.01377.x.
63. Sonnby-Borgstrom M. Automatic mimicry reactions as related to differences in emotional empathy. Scandinavian Journal of Psychology 2002, 43(5):433-443.
64. Soussignan R. Duchenne smile, emotional experience, and autonomic reactivity: a test of the facial feedback hypothesis. Emotion (Washington, D.C.) 2002, 2(1):52-74. 10.1037/1528-3542.2.1.52.
65. Stel M., van Knippenberg A. The role of facial mimicry in the recognition of affect. Psychological Science 2008, 19(10):984-985.
66. Stevens J.S., Hamann S. Sex differences in brain activation to emotional stimuli: a meta-analysis of neuroimaging studies. Neuropsychologia 2012, 50(7):1578-1593. 10.1016/j.neuropsychologia.2012.03.011.
67. Strack F., Martin L.L., Stepper S. Inhibiting and facilitating conditions of the human smile: a nonobtrusive test of the facial feedback hypothesis. Journal of Personality and Social Psychology 1988, 54(5):768-777.
68. Van der Gaag C., Minderaa R.B., Keysers C. Facial expressions: what the mirror neuron system can and cannot tell us. Social Neuroscience 2007, 2(3-4):179-222.
69. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 1988, 54(6):1063-1070.
70. Wollmer M.A., de Boer C., Kalak N., Beck J., Götz T., Schmidt T., et al. Facing depression with botulinum toxin: a randomized controlled trial. Journal of Psychiatric Research 2012, 46(5):574-581. 10.1016/j.jpsychires.2012.01.027.