Temporal dynamics of motor cortex excitability during perception of natural emotional scenes

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 10, 2014, Pages 1451-1457

  Borgomaneri, Sara ^a,b   Gazzola, Valeria ^a,c   Avenanti, Alessio ^b,d,e  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e Centro Studi e Ricerche in Neuroscienze Cognitive   (Italy)

Author keywords

Corticospinal excitability; Emotional scenes; Motor reactions; Neural dynamics; Personal distress; Transcranial magnetic stimulation

Indexed keywords

ADULT; ANALYSIS OF VARIANCE; DECISION MAKING; ELECTROMYOGRAPHY; EMOTION; FEMALE; HAND; HUMAN; INNERVATION; MALE; MOTOR CORTEX; MOTOR EVOKED POTENTIAL; PHOTOSTIMULATION; PHYSIOLOGY; STATISTICS; TRANSCRANIAL MAGNETIC STIMULATION; VISION; YOUNG ADULT;

ADULT; ANALYSIS OF VARIANCE; ELECTROMYOGRAPHY; EMOTIONS; EVOKED POTENTIALS, MOTOR; FEMALE; HAND; HUMANS; JUDGMENT; MALE; MOTOR CORTEX; PHOTIC STIMULATION; STATISTICS AS TOPIC; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84922925134     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst139     Document Type: Article

References (101)

1. Avenanti, A., Annela, L., Serino, A. (2012a). Suppression of premotor cortex disrupts motor coding of peripersonal space. Neuroimage, 63, 281-8.
2. Avenanti, A., Annella, L., Candidi, M., Urgesi, C., Aglioti, S.M. (2013a). Compensatory plasticity in the action observation network: virtual lesions of STS enhance anticipatory simulation of seen actions. Cerebral Cortex, 23, 570-80.
3. Avenanti, A., Bolognini, N., Maravita, A., Aglioti, S.M. (2007). Somatic and motor components of action simulation. Current Biology, 17, 2129-35.
4. Avenanti, A., Candidi, M., Urgesi, C. (2013b). Vicarious motor activation during action perception: beyond correlational evidence. Frontiers in Human Neuroscience, 7, 185.
5. Avenanti, A., Coccia, M., Ladavas, E., Provinciali, L., Ceravolo, M.G. (2012b). Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology, 78, 256-64.
6. Avenanti, A., Minio-Paluello, I., Bufalari, I., Aglioti, S.M. (2009a). The pain of a model in the personality of an onlooker: influence of state-reactivity and personality traits on embodied empathy for pain. Neuroimage, 44, 275-83.
7. Avenanti, A., Minio-Paluello, I., Sforza, A., Aglioti, S.M. (2009b). Freezing or escaping? Opposite modulations of empathic reactivity to the pain of others. Cortex, 45, 1072-7.
8. Avenanti, A., Sirigu, A., Aglioti, S.M. (2010). Racial bias reduces empathic sensorimotor resonance with other-race pain. Current Biology, 20, 1018-22.
9. Azevedo, R.T., Macaluso, E., Avenanti, A., Santangelo, V., Cazzato, V., Aglioti, S.M. (2013). Their pain is not our pain: Brain and autonomic correlates of empathic resonance with the pain of same and different race individuals. Human Brain Mapping, 34(12), 3168-81.
10. Barchiesi, G., Cattaneo, L. (2013). Early and late motor responses to action observation. Social Cognitive Affective Neuroscience, 8, 711-4.
11. Batson, C.D., Polycarpou, M.P., Harmon-Jones, E., et al. (1997). Empathy and attitudes: can feeling for a member of a stigmatized group improve feelings toward the group? Journal of Personality and Social Psychology, 72, 105-18.
12. Baumgartner, T., Willi, M., Jäncke, L. (2007). Modulation of corticospinal activity by strong emotions evoked by pictures and classical music: a transcranial magnetic stimulation study. NeuroReport, 18, 261-5.
13. Borgomaneri, S., Gazzola, V., Avenanti, A. (2012). Motor mapping of implied actions during perception of emotional body language. Brain Stimulation, 5, 70-6.
14. Borod, J.C. (2000). The Neuropsychology of Emotion. New York: Oxford University Press.
15. Bradley, M.M., Codispoti, M., Cuthbert, B.N., Lang, P.J. (2001). Emotion and motivation I: defensive and appetitive reactions in picture processing. Emotion, 1, 276-98.
16. Briggs, G.G., Nebes, R.D. (1975). Patterns of hand preference in a student population. Cortex, 11, 230-8.
17. Cacioppo, J., Priester, J.R., Berntson, G.G. (1993). Rudimentary determinants of attitudes. II: arm flexion and extension have differential affects on attitudes. Journal of Personality and Social Psychology, 65, 5-17.
18. Carretié, L., Albert, J., López-Martín, S., Tapia, M. (2009). Negative brain: an integrative review on the neural processes activated by unpleasant stimuli. International Journal of Psychophysiology, 71, 57-63.
19. Carretié, L., Hinojosa, J.A., Albert, J., Mercado, F. (2006). Neural response to sustained affective visual stimulation using an indirect task. Experimental Brain Research, 174, 630-7.
20. Carretié, L., Martín-Loeches, M., Hinojosa, J.A., Mercado, F. (2001). Attention and emotion interaction studied through event related potentials. Journal of Cognitive Neuroscience, 13, 1109-28.
21. Cavada, C., Compañy, T., Tejedor, J., Cruz-Rizzolo, R.J., Reinoso-Suárez, F. (2000). The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cerebral Cortex, 10, 220-42.
22. Chen, R., Classen, J., Gerloff, C., et al. (1997). Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology, 48, 1398-403.
23. Codispoti, M., Ferrari, V., Bradley, M.M. (2007). Repetition and event-related potentials: distinguishing early and late processes in affective picture perception. Journal of Cognitive Neuroscience, 19, 577-86.
24. Coombes, S.A., Janelle, C.M., Duley, A.R. (2005). Emotion and motor control: movement attributes following affective picture processing. Journal of Motor Behavior, 37, 425-36.
25. Coombes, S.A., Tandonnet, C., Fujiyama, H., Janelle, C.M., Cauraugh, J.H., Summers, J.J. (2009). Emotion and motor preparation: a transcranial magnetic stimulation study of corticospinal motor tract excitability. Cognitive and Affective Behavioral Neuroscience, 9, 380-8.
26. Cuthbert, B.N., Schupp, H.T., Bradley, M.M., Birbaumer, N., Lang, P.J. (2000). Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biological Psychology, 52, 95-111.
27. Darwin, C. (1872/1965). The Expressions of Emotions in Man and Animals. London, UK: John Murray. Reprint. Chicago: University of Chicago Press.
28. Davidson, R.J., Hugdahl, K. (1995). Brain Asymmetry. Cambridge, MA: MIT Press.
29. Davis, M.H. (1996). Empathy: A Social Psychological Approach. Boulder, CO: Westview Press.
30. de Gelder, B., van Honk, J., Tamietto, M. (2011). Emotion in the brain: of low roads, high roads and roads less travelled. Nature Reviews Neuroscience, 12, 425.
31. de Oliveira, L.A., Imbiriba, L.A., Russo, M.M., et al. (2012). Preparing to grasp emotionally laden stimuli. PLoS One, 7, e45235.
32. Enticott, P.G., Harrison, B.A., Arnold, S.L., et al. (2012). Emotional valence modulates putative mirror neuron activity. Neuroscience Letters, 508, 56-9.
33. Fadiga, L., Buccino, G., Craighero, L., Fogassi, L., Gallese, V., Pavesi, G. (1999). Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia, 37, 147-58.
34. Fadiga, L., Craighero, L., Olivier, E. (2005). Human motor cortex excitability during the perception of others' action. Current Opinion in Neurobiology, 15, 213-8.
35. Ferri, F., Ebisch, S.J., Costantini, M., et al. (2013). Binding action and emotion in social understanding. PLoS One, 8, e54091.
36. Ferri, F., Stoianov, I.P., Gianelli, C., D'Amico, L., Borghi, A.M., Gallese, V. (2010). When action meets emotions: how facial displays of emotion influence goal-related behavior. PLoS One, 5, e13126.
37. Fourkas, A.D., Avenanti, A., Urgesi, C., Aglioti, S.M. (2006). Corticospinal facilitation during first and third person imagery. Experimental Brain Research, 168, 143-51.
38. Fourkas, A.D., Bonavolontà, V., Avenanti, A., Aglioti, S.M. (2008). Kinesthetic imagery and tool-specific modulation of corticospinal representations in expert tennis players. Cerebral Cortex, 18, 2382-90.
39. Fox, E., Lester, V., Russo, R., Bowles, R.J., Pichler, A., Dutton, K. (2000). Facial expressions of emotion: are angry faces detected more efficiently? Cognition & Emotion, 14, 61-92.
40. Freina, L., Baroni, G., Borghi, A.M., Nicoletti, R. (2009). Emotive concept nouns and motor responses: attraction or repulsion? Memory & Cognition, 37, 493-9.
41. Frijda, N.H. (2009). Emotion experience and its varieties. Emotion Reviews, 1, 264-71.
42. Gazzola, V., Aziz-Zadeh, L., Keysers, C. (2006). Empathy and the somatotopic auditory mirror system in humans. Current Biology, 16, 1824-9.
43. Grecucci, A., Balaban, E., Buiatti, T., Budai, R., Rumiati, R.I. (2009). The emotional control of action: ERP evidence. Archives Italiennes de Biologie, 147, 37-49.
44. Grecucci, A., Koch, I., Rumiati, R.I. (2011). The role of emotional context in facilitating imitative actions. Acta Psychologica (Amst), 138, 311-5.
45. Gur, R.C., Schroeder, L., Turner, T., et al. (2002). Brain activation during facial emotion processing. Neuroimage, 16, 651-2.
46. Habel, U., Windischberger, C., Derntl, B., et al. (2007). Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. Neuropsychologia, 45, 2369-77.
47. Hajcak, G., Molnar, C., George, M.S., Bolger, K., Koola, J., Nahas, Z. (2007). Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. Psychophysiology, 44, 91-7.
48. Hajcak, G., Moser, J.S., Simons, R.F. (2006). Attending to affect: appraisal strategies modulate the electrocortical response to arousing pictures. Emotion, 6, 517-22.
49. Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron, 55, 187-99.
50. Hansen, C.H., Hansen, R.D. (1988). Finding the face in the crowd: an anger superiority effect. Journal of Personality and Social Psychology, 54, 917-24.
51. Hariri, A.R., Mattay, V.S., Tessitore, A., Fera, F., Weinberger, D.R. (2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry, 53, 494-501.
52. Hasbroucq, T., Kaneko, H., Akamatsu, M., Possamai, C.A. (1999). The time-course of preparatory spinal and cortico-spinal inhibition: an H-reflex and transcranial magnetic stimulation study in man. Experimental Brain Research, 124, 33-41.
53. Hoshiyama, M., Kakigi, R., Koyama, S., Takeshima, Y., Watanabe, S., Shimojo, M. (1997). Temporal changes of pyramidal tract activities after decision of movement: a study using transcranial magnetic stimulation of the motor cortex in humans. Electroencephalography and Clinical Neurophysiology, 105, 255-61.
54. Jabbi, M., Swart, M., Keysers, C. (2007). Empathy for positive and negative emotions in the gustatory cortex. Neuroimage, 34, 1744-53.
55. Kawasaki, H., Adolphs, R., Kaufman, O., et al. (2001). Single neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex. Nature Neuroscience, 4, 15-6.
56. Keil, A., Bradley, M.M., Hauk, O., Rockstroh, B., Elbert, T., Lang, P.J. (2002). Large-scale neural correlates of affective picture processing. Psychophysiology, 39, 641-9.
57. Koganemaru, S., Domen, K., Fukuyama, H., Mima, T. (2012). Negative emotion can enhance human motor cortical plasticity. European Journal of Neuroscience, 35, 1637-45.
58. Kret, M.E., Denollet, J., Grèzes, J., de Gelder, B. (2011). The role of negative affectivity and social inhibition in perceiving social threat: an fMRI study. Neuropsychologia, 49, 1187-93.
59. Lamm, C., Batson, C.D., Decety, J. (2007). The neural substrate of human empathy: effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19, 42-58.
60. Lamm, C., Porges, E.C., Cacioppo, J.T., Decety, J. (2008). Perspective taking is associated with specific facial responses during empathy for pain. Brain Research, 1227, 153-61.
61. Lang, P.J., Bradley, M.M., Cuthbert, B.N. (1999). International Affective Picture System: Instruction manual and affective ratings (Technial Report A-4). Gainsville, FL: University of Florida, The Center for Research in Psychophysiology.
62. Lang, P.J., Davis, M., Öhman, A. (2000). Fear and anxiety: animal models and human cognitive psychophysiology. Journal of Affective Disorders, 61, 137-59.
63. Lawrence, E.J., Shaw, P., Giampietro, V.P., Surguladze, S., Brammer, M.J., David, A.S. (2006). The role of 'shared representations' in social perception and empathy: an fMRI study. Neuroimage, 29, 1173-84.
64. Lepage, J.F., Tremblay, S., Théoret, H. (2010). Early non-specific modulation of corticospinal excitability during action observation. European Journal of Neuroscience, 31, 931-7.
65. Massaro, D.W., Cohen, M.M. (1995). Continuous versus discrete information processing in pattern recognition. Acta Psychologica (Amst), 90, 193-209.
66. Meister, I.G., Boroojerdi, B., Foltys, H., Sparing, R., Huber, W., Töpper, R. (2003). Motor cortex hand area and speech: implications for the development of language. Neuropsychologia, 41, 401-6.
67. Michelet, T., Duncan, G.H., Cisek, P. (2010). Response competition in the primary motor cortex: corticospinal excitability reflects response replacement during simple decisions. Journal of Neurophysiology, 104, 119-27.
68. Mikhailova, E.S., Bogomolova, I.V. (2000). Evoked cerebral cortex activity in the human brain in conditions of the active and passive perception of facial expressions. Neuroscience and Behavioral Physiology, 30, 679-85.
69. Miller, J.O., Riehle, A., Requin, J. (1992). Effects of preliminary perceptual output on neuronal activity of the primary motor cortex. Journal of Experimental Psychology: Human Perception & Performance, 18, 1121-38.
70. Minio-Paluello, I., Avenanti, A., Aglioti, S.M. (2006). Left hemisphere dominance in reading the sensory qualities of others' pain? Social Neuroscience, 1, 320-33.
71. Minio-Paluello, I., Baron Cohen, S., Avenanti, A., Walsh, V., Aglioti, S.M. (2009). Absence of embodied empathy during pain observation in Asperger Syndrome. Biological Psychiatry, 65, 55-62.
72. Morecraft, R.J., Van Hoesen, G.W. (1998). Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Research Bulletin, 45, 209-32.
73. Morelli, S.A., Rameson, L.T., Lieberman, M.D. (2014). The neural components of empathy: predicting daily prosocial behavior. Social Cognitive Affective Neuroscience, 9(1), 39-47.
74. Moriguchi, Y., Ohnishi, T., Lane, R.D., et al. (2006). Impaired self-awareness and theory of mind: an fMRI study of mentalizing in alexithymia. Neuroimage, 32, 1472-82.
75. Naugle, K.M., Joyner, J., Hass, C.J., Janelle, C.M. (2010). Emotional influences on locomotor behavior. Journal of Biomechanics, 43, 3099-103.
76. Northoff, G., Richter, A., Gessner, M., et al. (2000). Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. Cerebral Cortex, 10, 93-107.
77. Öhman, A., Mineka, S. (2001). Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychological Review, 108, 483-522.
78. Öhman, A., Flykt, A., Esteves, F. (2001). Emotion drives attention: detecting the snake in the grass. Journal of Experimental Psychology: General, 130, 466-78.
79. Oliveri, M., Babiloni, C., Filippi, M.M., et al. (2003). Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues. Experimental Brain Research, 149, 214-21.
80. Olofsson, J.K., Nordin, S., Sequeira, H., Polich, J. (2008). Affective picture processing: an integrative review of ERP findings. Biological Psychology, 77, 247-65.
81. Oya, H., Kawasaki, H., Howard, M.A. 3rd., Adolphs, R. (2002). Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. Journal of Neuroscience, 22, 9502-12.
82. Pessoa, L., Adolphs, R. (2010). Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nature Reviews Neuroscience, 11, 773-83.
83. Pourtois, G., Grandjean, D., Sander, D., Vuilleumier, P. (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex, 14, 619-33.
84. Prabhu, G., Voss, M., Brochier, T., Cattaneo, L., Haggard, P., Lemon, R. (2007). Excitability of human motor cortex inputs prior to grasp. Journal of Physiology, 581, 189-201.
85. Rossi, S., Hallett, M., Rossini, P.M., Pascual-Leone, A., Safety of TMS Consensus Group. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120, 2008-39.
86. Rossini, P.M., Barker, A.T., Berardelli, A., et al. (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalography and Clinical Neurophysiology, 91, 79-92.
87. Rotshtein, P., Richardson, M.P., Winston, J.S., et al. (2010). Amygdala damage affects event-related potentials for fearful faces at specific time windows. Human Brain Mapping, 31, 1089-105.
88. Saarela, M.V., Hlushchuk, Y., Williams, A.C., Schürmann, M., Kalso, E., Hari, R. (2007). The compassionate brain: humans detect intensity of pain from another's face. Cerebral Cortex, 17, 230-7.
89. Sabatinelli, D., Fortune, E.E., Li, Q., et al. (2011). Emotional perception: meta-analyses of face and natural scene processing. Neuroimage, 54, 2524-33.
90. Schupp, H.T., Junghöfer, M., Weike, A.I., Hamm, A.O. (2003). Emotional facilitation of sensory processing in the visual cortex. Psychological Science, 14, 7-13.
91. Serino, A., Annella, L., Avenanti, A. (2009). Motor properties of peripersonal space in humans. PLoS One, 4, e6582.
92. Silberman, E.K., Weingartner, H. (1986). Hemispheric lateralization of functions related to emotion. Brain Cognition, 5, 322-53.
93. Smith, N.K., Cacioppo, J.T., Larsen, J.T., Chartrand, T.L. (2003). May I have your attention, please: electrocortical responses to positive and negative stimuli. Neuropsychologia, 41, 171-83.
94. Tamietto, M., de Gelder, B. (2010). Neural bases of the non-conscious perception of emotional signals. Nature Reviews Neuroscience, 11, 697-709.
95. Tamietto, M., Castelli, L., Vighetti, S., et al. (2009). Unseen facial and bodily expressions trigger fast emotional reactions. Proceedings of the National Academy of Sciences of the United States of America, 106, 17661-6.
96. Tidoni, E., Borgomaneri, S., di Pellegrino, G., Avenanti, A. (2013). Action simulation plays a critical role in deceptive action recognition. Journal of Neuroscience, 33, 611-23.
97. Tokimura, H., Tokimura, Y., Oliviero, A., Asakura, T., Rothwell, J.C. (1996). Speechinduced changes in corticospinal excitability. Annals of Neurology, 40, 628-34.
98. Urgesi, C., Maieron, M., Avenanti, A., Tidoni, E., Fabbro, F., Aglioti, S.M. (2010). Simulating the future of actions in the human corticospinal system. Cerebral Cortex, 20, 2511-21.
99. van Loon, A.M., van den Wildenberg, W.P., van Stegeren, A.H., Hajcak, G., Ridderinkhof, K.R. (2010). Emotional stimuli modulate readiness for action: a transcranial magnetic stimulation study. Cognitive and Affective Behavioral Neuroscience, 10, 174-81.
100. Vuilleumier, P. (2002). Facial expression and selective attention. Current Opinion in Psychiatry, 15, 291-300.
101. Wassermann, E.M., Greenberg, B.D., Nguyen, M.B., Murphy, D.L. (2001). Motor cortex excitability correlates with an anxiety-related personality trait. Biological Psychiatry, 50, 377-82.