Modulation of the human mirror neuron system during cognitive activity
Suresh D. Muthukumaraswamy,
Krish D. Singh,
Suresh D. Muthukumaraswamy
CUBRIC (Cardiff University Brain Research Imaging Centre), School of Psychology, Cardiff University, Park Place, Cardiff CF103AT, United Kingdom
Search for more papers by this authorKrish D. Singh
CUBRIC (Cardiff University Brain Research Imaging Centre), School of Psychology, Cardiff University, Park Place, Cardiff CF103AT, United Kingdom
Search for more papers by this authorSuresh D. Muthukumaraswamy,
Krish D. Singh,
Suresh D. Muthukumaraswamy
CUBRIC (Cardiff University Brain Research Imaging Centre), School of Psychology, Cardiff University, Park Place, Cardiff CF103AT, United Kingdom
Search for more papers by this authorKrish D. Singh
CUBRIC (Cardiff University Brain Research Imaging Centre), School of Psychology, Cardiff University, Park Place, Cardiff CF103AT, United Kingdom
Search for more papers by this authorAddress reprint requests to: Suresh D. Muthukumaraswamy, CUBRIC (Cardiff University Brain Research Imaging Centre), School of Psychology, Cardiff University, Park Place, Cardiff CF103AT, United Kingdom. E-mail: [email protected]
Krish Singh is supported by the Biotechnology and Biological Sciences Research Council (BBSRC).
Abstract
In this experiment we examined the relationship between the mirror neuron system and increased attention caused by task demands. Whole head MEG recordings were made from 13 participants who were asked to passively observe finger movement sequences, observe these sequences with the knowledge they would later have to perform the sequence presented, and finally, to perform a nonmotor mathematics task based on the finger-movement sequences. Beta-band (15–35 Hz) sensorimotor desynchronization was found in overlapping areas during passive observation and in a separate motor execution condition, indicating the activity of the human mirror neuron system. The beta desynchronization in these areas was enhanced relative to passive viewing when participants had to watch the stimuli to later imitate and when they performed the mathematics task, indicating that mirror neuron system activity can be modulated by attention.
REFERENCES
- Aziz-Zadeh, L., Koski, L., Zaidel, E., Mazziotta, J., & Iacoboni, M. (2006). Lateralization of the human mirror neuron system. Journal of Neuroscience, 26, 2964–2970.
- Babiloni, C., Babiloni, F., Carducci, F., Cincotti, F., Cocozza, G., Del Percio, C., et al. (2002). Human cortical electroencephalography (EEG) rhythms during the observation of simple aimless movements: A high-resolution EEG study. NeuroImage, 17, 559–572.
- Bernier, R., Dawson, G., Webb, S., & Murias, M. (2007). EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder. Brain and Cognition, 64, 228–237.
-
Braitenberg, V., & Schuz, A. (1991). Anatomy of the cortex: Statistics and geometry. New York: Springer.
10.1007/978-3-662-02728-8 Google Scholar
- Brookes, M. J., Gibson, A. M., Hall, S. D., Furlong, P. L., Barnes, G. R., Hillebrand, A., et al. (2005). GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS co-localisation with fMRI BOLD response in visual cortex. NeuroImage, 26, 302–308.
- Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., et al. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study. European Journal of Neuroscience, 13, 400–404.
- Buccino, G., Vogt, S., Ritzl, A., Fink, G. R., Zilles, K., Freund, H. J., et al. (2004). Neural circuits underlying imitation learning of hand actions: An event-related fMRI study. Neuron, 42, 323–334.
- Chau, W., McIntosh, A. R., Robinson, S. E., Schulz, M., & Pantev, C. (2004). Improving permutation test power for group analysis spatically filtered MEG data. NeuroImage, 23, 983–996.
- Cheyne, D., Gaetz, W., Garnero, L., Lachaux, J.-P., Ducorps, A., Schwartz, D., et al. (2003). Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. Cognitive Brain Research, 17, 599–611.
- Cochin, S., Barthelemy, C., Roux, S., & Martineau, J. (1999). Observation and execution of movement: Similarities demonstrated by quantified electroencephalography. European Journal of Neuroscience, 11, 1839–1842.
- Creutzfeldt, O., & Houchin, J. (1974). Neuronal basis of EEG waves. In A. Redmond (Ed.), Handbook of electroencephalography and clinical neurophysiology (pp. 5–55). Amsterdam: Elsevier.
- Decety, J., Grezes, J., Costes, N., Perani, D., Jeannerod, W., Procyk, E., et al. (1997). Brain activity during observation of actions. Brain, 120, 1763–1777.
- Fogassi, L., Ferrari, P. F., Gesierich, B., Rozzi, S., Chersi, F., & Rizzolatti, G. (2005). Parietal lobe: From action organization to intention understanding. Science, 308, 662–667.
-
Gallese, V. (2005). Embodied simulation: From neurons to phenomenal experience.
Phenomenology and the Cognitive Sciences, 4, 23–28.
10.1007/s11097-005-4737-z Google Scholar
- Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609.
- Gazzola, V., Rizzolatti, G., Wicker, B., & Keysers, C. (2007). The anthropomorphic brain: The mirror neuron system responds to human and robotic actions. NeuroImage, 35, 1674–1684.
- Gusnard, D. A., Akbudak, E., Shulman, G. L., & Raichle, M. E. (2001). Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proceedings of the National Academy of Sciences, USA, 98, 4259–4264.
- Gusnard, D. A., & Raichle, M. E. (2001). Searching for a baseline: Functional imaging and the resting human brain. Nature Reviews Neuroscience, 2, 685–694.
- Hamalainen, M., Hari, R., Ilmoniemi, R. J., Knuutila, J., & Lounasmaa, O. V. (1993). Magnetoencephalography—Theory, instrumentation, and applications to noninvasive studies of the working human brain. Reviews of Modern Physics, 65, 413–497.
- Hari, R., Salmelin, R., Makela, J. P., Salenius, S., & Helle, M. (1997). Magnetoencephalographic cortical rhythms. International Journal of Psychophysiology, 26, 51–62.
- Hillebrand, A., Singh, K. D., Holliday, I., Furlong, P. L., & Barnes, G. R. (2005). A new approach to neuroimaging with magnetoencephalography. Human Brain Mapping, 25, 199–211.
- Honaga, E., Ukai, S., Ishii, R., Kawaguchi, S., Yamamoto, M., Ogawa, A., et al. (2004). Neuromagnetic oscillatory responses related to the mirror neuron system. International Congress Series, 1270, 229–232.
- Jacob, P., & Jeannerod, M. (2005). The motor theory of social cognition: A critique. Trends in Cognitive Sciences, 9, 21–25.
- Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156.
- Kilner, J. M., Vargas, C., Duval, S., Blakemore, S. J., & Sirigu, A. (2004). Motor activation prior to observation of a predicted movement. Nature Neuroscience, 7, 1299–1301.
- Klimesch, W. (1996). Memory processes, brain oscillations and EEG synchronization. International Journal of Psychophysiology, 24, 61–100.
- Klimesch, W., Doppelmayr, M., Schwaiger, J., Auinger, P., & Winkler, T. (1999). ‘Paradoxical’ alpha synchronization in a memory task. Cognitive Brain Research, 7, 493–501.
- Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, E. S., Rainey, L., et al. (2000). Automated Talairach Atlas labels for functional brain mapping. Human Brain Mapping, 10, 120–131.
- Lau, H. C., Rogers, R. D., Haggard, P., & Passingham, R. E. (2004). Attention to intention. Science, 303, 1208–1210.
- Lepage, J. F., & Theoret, H. (2006). EEG evidence for the presence of an action observation-execution matching system in children. European Journal of Neuroscience, 23, 2505–2510.
-
Lorento de No, R. (1947). Action potential of the motoneurons of the hypoglossal nucleus.
Journal of Cellular and Comparative Physiology, 29, 207–287.
10.1002/jcp.1030290303 Google Scholar
- Lotze, M., Montoya, P., Erb, M., Hulsmann, E., Flor, H., Klose, U., et al. (1999). Activation of cortical and cerebellar motor areas during executed and imagined hand movements: An fMRI study. Journal of Cognitive Neuroscience, 11, 491–501.
- Mukamel, R., Gelbard, H., Arieli, A., Hasson, U., Fried, I., & Malach, R. (2007). Coupling between neuronal firing, field potentials, and fMRI in human auditory cortex. Science, 309, 951–954.
- Murakami, S., & Okada, Y. (2006). Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals. Journal of Physiology, 575, 925–936.
- Muthukumaraswamy, S. D., & Johnson, B. W. (2004). Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology, 41, 152–156.
- Muthukumaraswamy, S. D., & Johnson, B. W. (2007). A dual mechanism neural framework for social understanding. Philosophical Psychology, 20, 43–63.
- Muthukumaraswamy, S. D., Johnson, B. W., Gaetz, W., & Cheyne, D. (2004). Neuromagnetic imaging reveals primary cortex activation during the observation of oro-facial movements. Neurology and Clinical Neurophysiology, 2, 1–4.
- Muthukumaraswamy, S. D., Johnson, B. W., Gaetz, W. C., & Cheyne, D. O. (2006). Neural processing of observed oro-facial movements reflects multiple action encoding strategies in the human brain. Brain Research, 1071, 105–112.
- Muthukumaraswamy, S. D., Johnson, B. W., & McNair, A. (2004). Mu rhythm modulation during observation of an object-directed grasp. Cognitive Brain Research, 19, 195–201.
- Muthukumaraswamy, S. D., & Singh, K. D. (2008). Spatiotemporal frequency tuning of BOLD and gamma band MEG responses compared in primary visual cortex. NeuroImage, 40, 1552–1560.
- Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapping, 15, 1–25.
- Nishitani, N., & Hari, R. (2000). Temporal dynamics of cortical representation for action. Proceedings of the National Academy of Sciences, USA, 97, 913–918.
- Nunez, P. L. (1981). Electric fields of the brain: The neurophysics of EEG. New York: Oxford University Press.
- Nunez, P. L., & Silberstein, R. B. (2000). On the relationship of synaptic activity to macroscopic measurements: Does co-registration of EEG with fMRI make sense? Brain Topography, 13, 79–96.
- 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.
- Oberman, L. M., Pineda, J. A., & Ramachandran, V. S. (2007). The human mirror neuron system: A link between action observation and social skills. Social Cognitive and Affective Neuroscience, 2, 62–66.
- Pfurtscheller, G. (1992). Event-related synchronization (ERS): An electrophysiological correlate of cortical areas at rest. Electroencephalography & Clinical Neurophysiology, 83, 62–69.
- Pfurtscheller, G., & Klimesch, W. (1990). Topographical display and interpretation of event-related desynchronization during a visual–verbal task. Brain Topography, 3, 85–93.
- Pfurtscheller, G., & Neuper, C. (1997). Motor imagery activates primary sensorimotor area in humans. Neuroscience Letters, 239, 65–68.
- Pineda, J. A. (2005). The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing”. Brain Research Reviews, 50, 57–68.
- Pineda, J. A., Allison, B. Z., & Vankov, A. (2000). The effects of self-movement, observation and imagination on μ rhythms and readiness potentials (RP's): Toward a brain-computer interface (BCI). IEEE Transactions on Rehabilitation Engineering, 8, 219–222.
- Rizzolatti, G., Camarda, R. M., Fogassi, L., Luppino, G., & Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Experimental Brain Research, 71, 491–507.
- Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192.
- Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Cognitive Brain Research, 3, 131–141.
- Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience, 2, 661–670.
- Rizzolatti, G., & Luppino, G. (2001). The cortical motor system. Neuron, 31, 889–901.
- Robinson, S. E., & Vrba, J. (1999). Functional neuroimaging by synthetic aperture manetometry (SAM). In T. Yoshimoto, M. Kotani, S. Kuriki, H. Karibe, & N. Nakasato (Eds.), Recent advances in biomagnetism (pp. 302–305). Sendai: Tohoku University Press.
- Salenius, S., Schnitzler, A., Salmelin, R., Jousmaki, V., & Hari, R. (1997). Modulation of human cortical rolandic rhythms during natural sensorimotor tasks. NeuroImage, 5, 221–228.
- Singh, K. D., Barnes, G. R., & Hillebrand, A. (2003). Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing. NeuroImage, 19, 1589–1601.
- Singh, K. D., Barnes, G. R., Hillebrand, A., Forde, E. M. E., & Williams, A. L. (2002). Task-related changes in cortical synchronization are spatially coincident with the hemodynamic response. NeuroImage, 16, 103–114.
- Strange, B. A., Otten, L. J., Josephs, O., Rugg, M. D., & Dolan, R. J. (2002). Dissociable human perirhinal, hippocampal, and parahippocampal roles during verbal encoding. Journal of Neuroscience, 22, 523–528.
- Tallon-Baudry, C., & Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends in Cognitive Sciences, 3, 151–162.
- Tanji, J., & Shima, K. (1996). Supplementary motor cortex in organization of movement. European Neurology, 36, 13–19.
- Vrba, J., & Robinson, S. E. (2001). Signal processing in magnetoencephalography. Methods, 25, 249–271.
Citing Literature
