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The effect of action observation/execution on mirror neuron system recruitment: an fMRI study in healthy individuals

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Abstract

Action observation and execution activate regions that are part of the motor and mirror neuron systems (MNS). Using functional magnetic resonance (fMRI), we defined the presence and extent of MNS activation during three different motor tasks with the dominant, right-upper limb in healthy individuals. The influence of the modality of task administration (execution, observation, observation and execution) was also investigated. fMRI scans during the execution (E) of a motor task, the observation (O) of a video showing the same task performed by another person and the simultaneous observation and execution (OE) of the task were obtained from three groups of healthy subjects (15 subjects per group) randomized to perform: a simple motor (SM) task, a complex motor (CM) task and a finalistic motor (FM) task. Manual dexterity was assessed using the 9-hole peg test and maximum finger tapping frequency. MNS activation was higher during FM than SM or CM tasks, independently from the modality of administration (E, O, or OE). Inferior frontal gyrus recruitment was more significant during SM than CM tasks in the E and O conditions. Compared to SM and FM, CM task resulted in increased recruitment of brain regions involved in complex motor task performance. Compared to O and E, OE resulted in the recruitment of additional, specific, brain areas in the cerebellum, temporal and parietal lobes. The modality of administration and the type of task modulated MNS recruitment during motor acts. This might have practical implications for the set-up of individualized motor rehabilitation strategies.

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References

  • Agnew, Z. K., Wise, R. J., & Leech, R. (2012). Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation. PloS one, 7, e32517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bellelli, G., Buccino, G., Bernardini, B., Padovani, A., & Trabucchi, M. (2010). Action observation treatment improves recovery of postsurgical orthopedic patients: evidence for a top-down effect? Archives of Physical Medicine and Rehabilitation, 91, 1489–1494.

    Article  PubMed  Google Scholar 

  • Biagi, L., Cioni, G., Fogassi, L., Guzzetta, A., & Tosetti, M. (2010). Anterior intraparietal cortex codes complexity of observed hand movements. Brain Research Bulletin, 81, 434–440.

    Article  PubMed  Google Scholar 

  • Buccino, G. (2014). Action observation treatment: a novel tool in neurorehabilitation. Philosophical Transactions of the Royal Society Of London. Series B, Biological Sciences, 369, 20130185.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. The European Journal of Neuroscience, 13, 400–404.

    CAS  PubMed  Google Scholar 

  • Buccino, G., Lui, F., Canessa, N., Patteri, I., Lagravinese, G., Benuzzi, F., et al. (2004a). Neural circuits involved in the recognition of actions performed by nonconspecifics: an FMRI study. Journal of Cognitive Neuroscience, 16, 114–126.

    Article  PubMed  Google Scholar 

  • Buccino, G., Vogt, S., Ritzl, A., Fink, G. R., Zilles, K., Freund, H. J., et al. (2004b). Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron, 42, 323–334.

    Article  CAS  PubMed  Google Scholar 

  • Buccino, G., Gatti, R., Giusti, M. C., Negrotti, A., Rossi, A., Calzetti, S., et al. (2011). Action observation treatment improves autonomy in daily activities in Parkinson's disease patients: results from a pilot study. Movement Disorders, 26, 1963–1964.

    Article  PubMed  Google Scholar 

  • Buccino, G., Arisi, D., Gough, P., Aprile, D., Ferri, C., Serotti, L., et al. (2012). Improving upper limb motor functions through action observation treatment: a pilot study in children with cerebral palsy. Developmental Medicine and Child Neurology, 54, 822–828.

    Article  PubMed  Google Scholar 

  • Calvo-Merino, B., Glaser, D. E., Grezes, J., Passingham, R. E., & Haggard, P. (2005). Action observation and acquired motor skills: an FMRI study with expert dancers. Cerebral Cortex, 15, 1243–1249.

    Article  CAS  PubMed  Google Scholar 

  • Calvo-Merino, B., Grezes, J., Glaser, D. E., Passingham, R. E., & Haggard, P. (2006). Seeing or doing? influence of visual and motor familiarity in action observation. Current Biology, 16, 1905–1910.

    Article  CAS  PubMed  Google Scholar 

  • Coynel, D., Marrelec, G., Perlbarg, V., Pelegrini-Issac, M., Van de Moortele, P. F., Ugurbil, K., et al. (2010). Dynamics of motor-related functional integration during motor sequence learning. NeuroImage, 49, 759–766.

    Article  PubMed  Google Scholar 

  • Duvernoy HM. (1999): The human brain. Surface, blood supply, and three-dimensional sectional anatomy. NewYork: SpringerWien.

  • Ertelt, D., Small, S., Solodkin, A., Dettmers, C., McNamara, A., Binkofski, F., et al. (2007). Action observation has a positive impact on rehabilitation of motor deficits after stroke. Neuroimage, 36(Suppl 2), T164–T173.

    Article  PubMed  Google Scholar 

  • Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: a magnetic stimulation study. Journal of Neurophysiology, 73, 2608–2611.

    CAS  PubMed  Google Scholar 

  • Friston, K. J., Holmes, A. P., Price, C. J., Buchel, C., & Worsley, K. J. (1999). Multisubject fMRI studies and conjunction analyses. NeuroImage, 10, 385–396.

    Article  CAS  PubMed  Google Scholar 

  • Gazzola, V. & Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cerebral Cortex, 19, 1239–1255.

    Article  PubMed  Google Scholar 

  • Goldenberg, G. & Karnath, H. O. (2006). The neural basis of imitation is body part specific. The Journal of Neuroscience, 26, 6282–6287.

    Article  CAS  PubMed  Google Scholar 

  • Grezes, J. (1998). Top down effect of strategy on the perception of human biological motion: a pet investigation. Cognitive Neuropsychology, 15, 553–582.

    Article  CAS  PubMed  Google Scholar 

  • Grezes, J., Armony, J. L., Rowe, J., & Passingham, R. E. (2003). Activations related to "mirror" and "canonical" neurones in the human brain: an fMRI study. NeuroImage, 18, 928–937.

    Article  CAS  PubMed  Google Scholar 

  • Iacoboni, M. & Mazziotta, J. C. (2007). Mirror neuron system: basic findings and clinical applications. Annals of Neurology, 62, 213–218.

    Article  PubMed  Google Scholar 

  • Iacoboni, M., Woods, R. P., Brass, M., Bekkering, H., Mazziotta, J. C., & Rizzolatti, G. (1999). Cortical mechanisms of human imitation. Science, 286, 2526–2528.

    Article  CAS  PubMed  Google Scholar 

  • Johnson-Frey, S. H., Maloof, F. R., Newman-Norlund, R., Farrer, C., Inati, S., & Grafton, S. T. (2003). Actions or hand-object interactions? human inferior frontal cortex and action observation. Neuron, 39, 1053–1058.

    Article  CAS  PubMed  Google Scholar 

  • Kessler, K., Biermann-Ruben, K., Jonas, M., Siebner, H. R., Baumer, T., Munchau, A., et al. (2006). Investigating the human mirror neuron system by means of cortical synchronization during the imitation of biological movements. NeuroImage, 33, 227–238.

    Article  PubMed  Google Scholar 

  • Leech, R., Braga, R., & Sharp, D. J. (2012). Echoes of the brain within the posterior cingulate cortex. The Journal of Neuroscience, 32, 215–222.

    Article  CAS  PubMed  Google Scholar 

  • Lingnau, A. & Downing, P. E. (2015). The lateral occipitotemporal cortex in action. Trends in Cognitive Sciences, 19, 268–277.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Newman-Norlund, R., van Schie, H. T., van Hoek, M. E., Cuijpers, R. H., & Bekkering, H. (2010). The role of inferior frontal and parietal areas in differentiating meaningful and meaningless object-directed actions. Brain Research, 1315, 63–74.

    Article  CAS  PubMed  Google Scholar 

  • Nishitani, N. & Hari, R. (2000). Temporal dynamics of cortical representation for action. Proceedings of the National Academy Of Sciences of the United States Of America, 97, 913–918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97–113.

    Article  CAS  PubMed  Google Scholar 

  • Plata Bello, J., Modrono, C., Marcano, F., & Gonzalez-Mora, J. L. (2013). Observation of simple intransitive actions: the effect of familiarity. PloS one, 8, e74485.

    Article  PubMed  PubMed Central  Google Scholar 

  • Plata Bello, J., Modrono, C., Marcano, F., & Gonzalez-Mora, J. L. (2014). The mirror neuron system and motor dexterity: what happens? Neuroscience, 275, 285–295.

    Article  CAS  PubMed  Google Scholar 

  • Plata Bello, J., Modrono, C., Marcano, F., & Gonzalez-Mora, J. L. (2015). The effect of motor familiarity during simple finger opposition tasks. Brain Imaging and Behavior, 9, 828–838.

    Article  PubMed  Google Scholar 

  • Porro, C. A., Facchin, P., Fusi, S., Dri, G., & Fadiga, L. (2007). Enhancement of force after action observation: behavioural and neurophysiological studies. Neuropsychologia, 45, 3114–3121.

    Article  PubMed  Google Scholar 

  • Rizzolatti, G. & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192.

    Article  CAS  PubMed  Google Scholar 

  • Rocca, M. A., Falini, A., Comi, G., Scotti, G., & Filippi, M. (2008). The mirror-neuron system and handedness: a "right" world? Human Brain Mapping, 29, 1243–1254.

    Article  PubMed  Google Scholar 

  • Romaiguere, P., Nazarian, B., Roth, M., Anton, J. L., & Felician, O. (2014). Lateral occipitotemporal cortex and action representation. Neuropsychologia, 56, 167–177.

    Article  PubMed  Google Scholar 

  • Shima, K. & Tanji, J. (1998). Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. Journal of Neurophysiology, 80, 3247–3260.

    CAS  PubMed  Google Scholar 

  • Stefan, K., Cohen, L. G., Duque, J., Mazzocchio, R., Celnik, P., Sawaki, L., et al. (2005). Formation of a motor memory by action observation. The Journal of Neuroscience, 25, 9339–9346.

    Article  CAS  PubMed  Google Scholar 

  • Stoodley, C. J. & Schmahmann, J. D. (2010). Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex, 46, 831–844.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanaka, S., Inui, T., Iwaki, S., Konishi, J., & Nakai, T. (2001). Neural substrates involved in imitating finger configurations: an fMRI study. Neuroreport, 12, 1171–1174.

    Article  CAS  PubMed  Google Scholar 

  • Vogt, S., Buccino, G., Wohlschlager, A. M., Canessa, N., Shah, N. J., Zilles, K., et al. (2007). Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise. NeuroImage, 37, 1371–1383.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Analysis and Rehabilitation of Motor Function San Raffaele Scientific Institute, Vita-Salute, Milan, Italy

    Roberto Gatti & Silvia Fumagalli

  2. Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute, Via Olgettina, 60, 20132, Milan, Italy

    Maria A. Rocca, Silvia Fumagalli & Massimo Filippi

  3. Faculty of Physical Education and Physiotherapy, Vrije Universiteit Brussel, Bruxelles, Belgium

    Erik Cattrysse & Eric Kerckhofs

  4. Department of Neuroradiology, San Raffaele Scientific Institute, Vita-Salute, Milan, Italy

    Andrea Falini

Authors
  1. Roberto Gatti
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  2. Maria A. Rocca
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  3. Silvia Fumagalli
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  4. Erik Cattrysse
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  5. Eric Kerckhofs
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  6. Andrea Falini
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  7. Massimo Filippi
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Corresponding author

Correspondence to Massimo Filippi.

Ethics declarations

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Funding

Partially supported by grants from FISM (FISM 2012/R/15) and the Italian Ministry of Health (RF-2011-02,350,374).

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Roberto Gatti and Maria A. Rocca contributed equally to this work.

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Gatti, R., Rocca, M.A., Fumagalli, S. et al. The effect of action observation/execution on mirror neuron system recruitment: an fMRI study in healthy individuals. Brain Imaging and Behavior 11, 565–576 (2017). https://doi.org/10.1007/s11682-016-9536-3

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