Abstract
In the present study, we examined the involvement of the extended mirror neuron system (MNS)—specifically, areas that have a strong functional connection to the core system itself—during emotional and nonemotional judgments about human song. We presented participants with audiovisual recordings of sung melodic intervals (two-tone sequences) and manipulated emotion and pitch judgments while keeping the stimuli identical. Mu event-related desynchronization (ERD) was measured as an index of MNS activity, and a source localization procedure was performed on the data to isolate the brain sources contributing to this ERD. We found that emotional judgments of human song led to greater amounts of ERD than did pitch distance judgments (nonemotional), as well as control judgments related to the singer’s hair, or pitch distance judgments about a synthetic tone sequence. Our findings support and expand recent research suggesting that the extended MNS is involved to a greater extent during emotional than during nonemotional perception of human action.
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References
Aragón, O. R., Sharer, E. A., Bargh, J. A., & Pineda, J. A. (2013). Modulations of mirroring activity by desire for social connection and relevance of movement. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nst172.
Barraclough, N. E., Xiao, D., Baker, C. I., Oram, M. W., & Perrett, D. I. (2005). Integration of visual and auditory information by superior temporal sulcus neurons responsive to the sight of actions. Journal of Cognitive Neuroscience, 17, 377–391. doi:10.1162/0898929053279586
Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., … Freund, H. J. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study. European Journal of Neuroscience, 13, 400–404.
Carr, L., Iacoboni, M., Dubeau, M.-C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences, 100, 5497–5502. doi:10.1073/pnas.0935845100
Casasanto, D., & Dijkstra, K. (2010). Motor action and emotional memory. Cognition, 115, 179–185.
Chan, L., Livingstone, S., & Russo, F. A. (2013). Automatic facial mimicry of emotion during perception of song. Music Perception, 30, 361–367.
Chartrand, T., & Bargh, J. (1999). The chameleon effect: The perception–behavior link and social interaction. Journal of Personality and Social Psychology, 76, 893–910.
Cheng, Y., Chou, K.-H., Decety, J., Chen, I.-Y., Hung, D., Tzeng, O. J.-L., & Lin, C.-P. (2009). Sex differences in the neuroanatomy of human mirror-neuron system: A voxel-based morphometric investigation. Neuroscience, 158, 713–720. doi:10.1016/j.neuroscience.2008.10.026
Cochin, S., Barthelemy, C., Lejeune, B., Roux, S., & Martineau, J. (1998). Perception of motion and qEEG activity in human adults. Electroencephalography and Clinical Neurophysiology, 107, 287–295.
Cross, E. S., Hamilton, A. F. D. C., & Grafton, S. T. (2006). Building a motor simulation de novo: Observation of dance by dancers. NeuroImage, 31, 1257–1267. doi:10.1016/j.neuroimage.2006.01.033
Dapretto, M., Davies, M. S., Pfeifer, J. H., Scott, A. A., Sigman, M., Bookheimer, S. Y., & Iacoboni, M. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9, 28–30. doi:10.1038/nn1611
Davidson, R. J. (1998). Anterior electrophysiological asymmetries, emotion, and depression: Conceptual and methodological conundrums. Psychophysiology, 35, 607–614.
Davidson, R. J., & Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Sciences, 3, 11–21.
Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134, 9–21. doi:10.1016/j.jneumeth.2003.10.009
Delorme, A., & Makeig, S. (2013). EEGlab wiki. Retrieved July 1, 2014, from http://sccn.ucsd.edu/wiki/Main_Page
di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91, 176–180. doi:10.1007/BF00230027
Dimberg, U., Thunberg, M., & Elmehed, K. (2000). Unconscious facial reactions to emotional facial expressions. Psychological Science, 11, 86–89. doi:10.1111/1467-9280.00221
Dinstein, I., Thomas, C., Behrmann, M., & Heeger, D. J. (2008). A mirror up to nature. Current Biology, 18, R13–R18.
Enticott, P. G., Johnston, P. J., Herring, S. E., Hoy, K. E., & Fitzgerald, P. B. (2008). Mirror neuron activation is associated with facial emotion processing. Neuropsychologia, 46, 2851–2854. doi:10.1016/j.neuropsychologia.2008.04.022
Ferri, F., Ebisch, S. J. H., Costantini, M., Salone, A., Arciero, G., Mazzola, V., Ferro, F. M., … Gallese, V. (2013). Binding action and emotion in social understanding. PLoS ONE, 8, e54091. doi:10.1371/journal.pone.0054091
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609.
Gazzaniga, M. S. (1995). Principles of human brain organization derived from split-brain studies. Neuron, 14, 217–228.
Gazzola, V., Aziz-Zadeh, L., & Keysers, C. (2006). Empathy and the somatotopic auditory mirror system in humans. Current Biology, 16, 1824–1829. doi:10.1016/j.cub.2006.07.072
George, M. S., Parekh, P. I., Rosinsky, N., Ketter, T. A., Kimbrell, T. A., Heilman, K. M., … Post, R. M. (1996). Understanding emotional prosody activates right hemisphere regions. Archives of Neurology, 53, 665–670. doi:10.1001/archneur.1996.00550070103017
Grosbras, M.-H., & Paus, T. (2006). Brain networks involved in viewing angry hands or faces. Cerebral Cortex, 16, 1087–1096. doi:10.1093/cercor/bhj050
Hari, R., Forss, N., Avikainen, S., Kirveskari, E., Salenius, S., & Rizzolatti, G. (1998). Activation of human primary motor cortex during action observation: A neuromagnetic study. Proceedings of the National Academy of Sciences, 95, 15061–15065.
Harris, T., Harris, S., Rubin, J. S., & Howard, D. M. (1998). The voice clinic handbook. London, UK: Whurr.
Hess, U., & Blairy, S. (2001). Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy. International Journal of Psychophysiology, 40, 129–141.
Iacoboni, M., Koski, L. M., Brass, M., Bekkering, H., Woods, R. P., Dubeau, M. C., … Rizzolatti, G. (2001). Reafferent copies of imitated actions in the right superior temporal cortex. Proceedings of the National Academy of Sciences, 98, 13995–13999.
Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J. C., & Rizzolatti, G. (2005). Grasping the intentions of others with one’s own mirror neuron system. PLoS Biology, 3, e79. doi:10.1371/journal.pbio.0030079
Iidaka, T. (2012). The role of the superior temporal sulcus in face recognition and perception [in Japanese]. Brain and Nerve, 64, 737–742.
Keysers, C., & Gazzola, V. (2009). Expanding the mirror: Vicarious activity for actions, emotions, and sensations. Current Opinion in Neurobiology, 19, 666–671. doi:10.1016/j.conb.2009.10.006
Keysers, C., Kohler, E., Umiltà, M. A., Nanetti, L., Fogassi, L., & Gallese, V. (2003). Audiovisual mirror neurons and action recognition. Experimental Brain Research, 153, 628–636. doi:10.1007/s00221-003-1603-5
Kreifelts, B., Ethofer, T., Shiozawa, T., Grodd, W., & Wildgruber, D. (2009). Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice-and face-sensitive regions in the superior temporal sulcus. Neuropsychologia, 47, 3059–3066.
LeDoux, J. E., & Phelps, E. A. (1993). Emotional networks in the brain. In M. Lewis, J. M. Haviland-Jones, & L. Feldman Barrett (Eds.), Handbook of emotions (pp. 159–179). New York, NY: Guilford Press.
Leff, A. P., Schofield, T. M., Crinion, J. T., Seghier, M. L., Grogan, A., Green, D. W., & Price, C. J. (2009). The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: Evidence from 210 patients with stroke. Brain, 132, 3401–3410.
Lévêque, Y., & Schön, D. (2013). Listening to the human voice alters sensorimotor brain rhythms. PLoS ONE, 8, e80659. doi:10.1371/journal.pone.0080659
McGarry, L. M., & Russo, F. A. (2011). Mirroring in dance/movement therapy: Potential mechanisms behind empathy enhancement. Arts in Psychotherapy, 38, 178–184. doi:10.1016/j.aip.2011.04.005
McGarry, L. M., Russo, F. A., Schalles, M. D., & Pineda, J. A. (2012). Audio-visual facilitation of the mu rhythm. Experimental Brain Research, 218, 527–538. doi:10.1007/s00221-012-3046-3
Mognon, A., Jovicich, J., Bruzzone, L., & Buiatti, M. (2011). ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. Psychophysiology, 48, 229–240.
Molenberghs, P., Brander, C., Mattingley, J. B., & Cunnington, R. (2010). The role of the superior temporal sulcus and the mirror neuron system in imitation. Human Brain Mapping, 31, 1316–1326. doi:10.1002/hbm.20938
Molenberghs, P., Cunnington, R., & Mattingley, J. B. (2012). Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies. Neuroscience and Biobehavioral Reviews, 36, 341–349. doi:10.1016/j.neubiorev.2011.07.004
Molnar-Szakacs, I., & Overy, K. (2006). Music and mirror neurons: From motion to “e”motion. Social Cognitive and Affective Neuroscience, 1, 235–241. doi:10.1093/scan/nsl029
Moody, E. J., & McIntosh, D. N. (2011). Mimicry of dynamic emotional and motor-only stimuli. Social Psychological and Personality Science, 2, 679–686. doi:10.1177/1948550611406741
Moore, A., Gorodnitsky, I., & Pineda, J. (2012). EEG mu component responses to viewing emotional faces. Behavioural Brain Research, 226, 309–316. doi:10.1016/j.bbr.2011.07.048
Mukamel, R., Ekstrom, A. D., Kaplan, J., Iacoboni, M., & Fried, I. (2010). Single-neuron responses in humans during execution and observation of actions. Current Biology, 20, 750–756. doi:10.1016/j.cub.2010.02.045
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, 24, 190–198. doi:10.1016/j.cogbrainres.2005.01.014
Overy, K., & Molnar-Szakacs, I. (2009). Being together in time: Musical experience and the mirror neuron system. Music Perception, 26, 489–504.
Perry, A., Troje, N. F., & Bentin, S. (2010). Exploring motor system contributions to the perception of social information: Evidence from EEG activity in the mu/alpha frequency range. Social Neuroscience, 5, 272–284. doi:10.1080/17470910903395767
Pfurtscheller, G., & Lopes da Silva, F. H. (1999). Event-related EEG/MEG synchronization and desynchronization: Basic principles. Clinical Neurophysiology, 110, 1842–1857.
Pineda, J. A. (2005). The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing.”. Brain Research Reviews, 50, 57–68. doi:10.1016/j.brainresrev.2005.04.005
Pineda, J. A. (2008). Sensorimotor cortex as a critical component of an “extended” mirror neuron system: Does it solve the development, correspondence, and control problems in mirroring? Behavioral and Brain Functions, 4, 47. doi:10.1186/1744-9081-4-47
Pineda, J. A., & Hecht, E. (2009). Mirroring and mu rhythm involvement in social cognition: Are there dissociable subcomponents of theory of mind ? Biological Psychology, 80, 306–314. doi:10.1016/j.biopsycho.2008.11.003
Redcay, E. (2008). The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism. Neuroscience and Biobehavioral Reviews, 32, 123–142. doi:10.1016/j.neubiorev.2007.06.004
Riskind, J. H., & Gotay, C. C. (1982). Physical posture: Could it have regulatory or feedback effects on motivation and emotion? Motivation and Emotion, 6, 273–298. doi:10.1007/BF00992249
Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192. doi:10.1146/annurev.neuro.27.070203.144230
Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Cognitive Brain Research, 3, 131–141.
Russo, F. A., Sandstrom, G. M., & Maksimowski, M. (2011). Mouth versus eyes: Gaze fixation during perception of sung interval size. Psychomusicology: Music, Mind and Brain, 21, 98–107. doi:10.1037/h0094007
Russo, F. A., & Thompson, W. F. (2005). The subjective size of melodic intervals over a two-octave range. Psychonomic Bulletin & Review, 12, 1068–1075. doi:10.3758/BF03206445
Sauseng, P., Klimesch, W., Stadler, W., Schabus, M., Doppelmayr, M., Hanslmayr, S., … Birbaumer, N. (2005). A shift of visual spatial attention is selectively associated with human EEG alpha activity. European Journal of Neuroscience, 22, 2917–2926.
Schellenberg, E. G., & Trehub, S. E. (1996). Children’s discrimination of melodic intervals. Developmental Psychology, 32, 1039–1050. doi:10.1037/0012-1649.32.6.1039
Scherer, K. R., & Oshinsky, J. S. (1977). Cue utilization in emotion attribution from auditory stimuli. Motivation and Emotion, 1, 331–346.
Schirmer, A., & Kotz, S. A. (2006). Beyond the right hemisphere: Brain mechanisms mediating vocal emotional processing. Trends in Cognitive Sciences, 10, 24–30. doi:10.1016/j.tics.2005.11.009
Schwartz, G. E., Davidson, R. J., & Maer, F. (1975). Right hemisphere lateralization for emotion in the human brain: Interactions with cognition. Science, 190, 286–288.
Singer, T., Seymour, B., O’Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science, 303, 1157–1162. doi:10.1126/science.1093535
Talmi, D., Luk, B. T. C., McGarry, L. M., & Moscovitch, M. (2007). The contribution of relatedness and distinctiveness to emotionally-enhanced memory. Journal of Memory and Language, 56, 555–574. doi:10.1016/j.jml.2007.01.002
Thompson, W. F., Russo, F. A., & Quinto, L. (2008). Audio–visual integration of emotional cues in song. Cognition and Emotion, 22, 1457–1470. doi:10.1080/02699930701813974
Umiltà, M. A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., & Rizzolatti, G. (2001). I know what you are doing: A neurophysiological study. Neuron, 31, 155–165. doi:10.1016/S0896-6273(01)00337-3
Wager, T. D., Phan, K. L., Liberzon, I., & Taylor, S. F. (2003). Valence, gender, and lateralization of functional brain anatomy in emotion: A meta-analysis of findings from neuroimaging. NeuroImage, 19, 513–531.
Warren, J. E., Sauter, D. A., Eisner, F., Wiland, J., Dresner, M. A., Wise, R. J. S., Rosen, S., … Scott, S. K. (2006). Positive emotions preferentially engage an auditory–motor “mirror” system. Journal of Neuroscience, 26, 13067–13075. doi:10.1523/JNEUROSCI.3907-06.2006
Watson, R., Latinus, M., Charest, I., Crabbe, F., & Belin, P. (2014). People-selectivity, audiovisual integration and heteromodality in the superior temporal sulcus. Cortex, 50, 125–136. doi:10.1016/j.cortex.2013.07.011
Wicker, B., Keysers, C., Plailly, J., Royet, J.-P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron, 40, 655–664. doi:10.1016/S0896-6273(03)00679-2
Williams, J. H. G., Waiter, G. D., Gilchrist, A., Perrett, D. I., Murray, A. D., & Whiten, A. (2006). Neural mechanisms of imitation and “mirror neuron” functioning in autistic spectrum disorder. Neuropsychologia, 44, 610–621. doi:10.1016/j.neuropsychologia.2005.06.010
Zaki, J., Weber, J., Bolger, N., & Ochsner, K. (2009). The neural bases of empathic accuracy. Proceedings of the National Academy of Sciences, 106, 11382–11387. doi:10.1073/pnas.0902666106
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This research was supported by a Canada Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada (NSERC) awarded to the first author and a Discovery grant from NSERC awarded to the third author. Additional funding was provided by Advancing Interdisciplinary Research in Singing (AIRS), a Major Collaborative Research Initiative funded by the Social Sciences and Humanities Research Council of Canada (www.airsplace.ca). Thank you to Emmalia Bortolon-Vettor and Tristan Defrancesco-Loria for assistance with data collection. The authors report no conflicts of interest.
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McGarry, L.M., Pineda, J.A. & Russo, F.A. The role of the extended MNS in emotional and nonemotional judgments of human song. Cogn Affect Behav Neurosci 15, 32–44 (2015). https://doi.org/10.3758/s13415-014-0311-x
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DOI: https://doi.org/10.3758/s13415-014-0311-x