The role of mirror neurons in observational motor learning: an integrative review

Authors

  • Angel Lago-Rodríguez
  • Binith Cheeran
  • Giacomo Koch
  • Tibor Hortobagy
  • Miguel Fernandez-del-Olmo

Abstract

Mirror neurons were discovered in the early 1990’s in the premotor cortex of the rhesus macaque. These  special, visuo-motor neurons discharge action potentials when executing an action, as well as during the observation of the performance of a similar action. During an observational motor learning protocol, learners acquire new motor patterns based on the visual information presented by an execution model. In order to do so, learners have to transform the observed visual information into motor commands (visuo-motor transformation). Studies show that observational motor learning may improve action perception and motor execution. Moreover, action perception and action execution interact in a mutual and bi-directional fashion (visuo-motor and motor-visual interaction), suggesting that perception and action share common neural mechanisms. Mirror neurons have been proposed as the neurophysiological basis of the visuo-motor and motor-visual transformation processes, and may play a role in the perceptual and motor improvements induced by observational motor learning.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Abernethy, B. (1990). Anticipation in squash: differences in advance cue utilization between expert and novice players. Journal of sports sciences, 8(1), 17-34.

Aglioti, S. M., Cesari, P., Romani, M., & Urgesi, C. (2008). Action anticipation and motor resonance in elite basketball players. Nature Neuroscience, 11(9), 1109-1116.

Al-Abood, S. A., Davids, K., Bennett, S. J., Ashford, D., & Martinez Marin, M. (2001). Effects of manipulating relative and absolute motion information during observational learning of an aiming task. J Sports Sci, 19(7), 507-520.

Al-Abood, S. A., Davids, K. F., & Bennett, S. J. (2001). Specificity of task constraints and effects of visual demonstrations and verbal instructions in directing learners' search during skill acquisition. J Mot Behav, 33(3), 295-305.

Avenanti, A., Bolognini, N., Maravita, A., & Aglioti, S. M. (2007). Somatic and motor components of action simulation. Curr Biol, 17(24), 2129-2135.

Avenanti, A., Bueti, D., Galati, G., & Aglioti, S. M. (2005). Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci, 8(7), 955-960.

Avenanti, A., Minio-Paluello, I., Bufalari, I., & Aglioti, S. M. (2006). Stimulus-driven modulation of motor-evoked potentials during observation of others' pain. Neuroimage, 32(1), 316-324.

Avenanti, A., Minio-Paluello, I., Sforza, A., & Aglioti, S. M. (2009). Freezing or escaping? Opposite modulations of empathic reactivity to the pain of others. Cortex, 45(9), 1072-1077.

Badets, A., Blandin, Y., & Shea, C. H. (2006). Intention in motor learning through observation. Quarterly Journal of Experimental Psychology, 59(2), 377-386.

Bandura, A. (1986). Social foundations of thought and action : a social cognitive theory. Englewood Cliffs, N.J.: Prentice-Hall.

Barzouka, K., Bergeles, N., & Hatziharistos, D. (2007). Effect of simultaneous model observation and self-modeling of volleyball skill acquisition. Percept Mot Skills, 104(1), 32-42.

Black, C. B., & Wright, D. L. (2000). Can observational practice facilitate error recognition and movement production? Research Quarterly For Exercise And Sport, 71(4), 331-339.

Borroni, P., Montagna, M., Cerri, G., & Baldissera, F. (2005). Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement. Brain Research, 1065(1-2), 115-124.

Borroni, P., Montagna, M., Cerri, G., & Baldissera, F. (2008). Bilateral motor resonance evoked by observation of a one-hand movement: role of the primary motor cortex. The European Journal Of Neuroscience, 28(7), 1427-1435.

Boschker, M. S., & Bakker, F. C. (2002). Inexperienced sport climbers might perceive and utilize new opportunities for action by merely observing a model. Percept Mot Skills, 95(1), 3-9.

Brass, M., Bekkering, H., Wohlschlager, A., & Prinz, W. (2000). Compatibility between observed and executed finger movements: comparing symbolic, spatial, and imitative cues. Brain Cogn, 44(2), 124-143.

Breslin, G., Hodges, N. J., Williams, A. M., Curran, W., & Kremer, J. (2005). Modelling relative motion to facilitate intra-limb coordination. Hum Mov Sci, 24(3), 446-463.

Brighina, F., La Bua, V., Oliveri, M., Piazza, A., & Fierro, B. (2000). Magnetic stimulation study during observation of motor tasks. J Neurol Sci, 174(2), 122-126.

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. The European Journal Of Neuroscience, 13(2), 400-404.

Buchanan, J. J., & Dean, N. J. (2010). Specificity in practice benefits learning in novice models and variability in demonstration benefits observational practice. Psychol Res, 74(3), 313-326.

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. Cereb Cortex, 15(8), 1243-1249.

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. Curr Biol, 16(19), 1905-1910.

Canal-Bruland, R., & Williams, A. M. (2010). Recognizing and predicting movement effects: identifying critical movement features. Exp Psychol, 57(4), 320-326.

Cattaneo, L., & Rizzolatti, G. (2009). The mirror neuron system. Archives of Neurology, 66(5), 557-560.

Cook R, Bird G, Catmur C, Press C, & Heyes C (2014). Mirror neurons: from origin to function. Behav Brain Sci, 37(2), 177-192.

Craighero, L., Bello, A., Fadiga, L., & Rizzolatti, G. (2002). Hand action preparation influences the responses to hand pictures. Neuropsychologia, 40(5), 492-502.

Craighero, L., Metta, G., Sandini, G., & Fadiga, L. (2007). The mirror-neurons system: data and models. Prog Brain Res, 164, 39-59.

Cross, E. S., Hamilton, A. F., & Grafton, S. T. (2006). Building a motor simulation de novo: observation of dance by dancers. Neuroimage, 31(3), 1257-1267.

di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp Brain Res, 91(1), 176-180.

Eidelberg, L. (1929). Experimenteller Beitrag zum Mechanismus der Imitationsbewegung. Jahresbücher für Psychiatrie und Neurologie 46, 170-173.

Enticott Peter G. , H. A. K., John L. Bradshaw, Nicole K. Rinehart, Paul B. Fitzgerald. (2010). Understanding mirror neurons: Evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures. Neuropsychologia.

Fabbri-Destro, M., & Rizzolatti, G. (2008). Mirror neurons and mirror systems in monkeys and humans. Physiology (Bethesda), 23, 171-179.

Fadiga, L., Craighero, L., & Olivier, E. (2005). Human motor cortex excitability during the perception of others' action. Curr Opin Neurobiol, 15(2), 213-218.

Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol, 73(6), 2608-2611.

Fecteau, S., Pascual-Leone, A., & Theoret, H. (2008). Psychopathy and the mirror neuron system: preliminary findings from a non-psychiatric sample. Psychiatry Res, 160(2), 137-144.

Ferrari, P. F., & Rizzolatti, G. (2014). Mirror neuron research: The past and the future. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1644).

Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119 ( Pt 2), 593-609.

Gangitano, M., Mottaghy, F. M., & Pascual-Leone, A. (2001). Phase-specific modulation of cortical motor output during movement observation. Neuroreport, 12(7), 1489-1492.

Gangitano, M., Mottaghy, F. M., & Pascual-Leone, A. (2004). Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci, 20(8), 2193-2202.

Goulet, C., Bard, C., & Fleury, M. (1989). Expertise differences in preparing to return a tennis serve: A visual information proccesing approach. Journal of Sport and Exercise Psychology, 11, 382-398.

Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron, 55(2), 187-199.

Hayes, S. J., Ashford, D., & Bennett, S. J. (2008). Goal-directed imitation: the means to an end. Acta Psychologica, 127(2), 407-415.

Hayes, S. J., Hodges, N. J., Scott, M. A., Horn, R. R., & Williams, A. M. (2006). Scaling a motor skill through observation and practice. J Mot Behav, 38(5), 357-366.

Hayes, S. J., Hodges, N. J., Scott, M. A., Horn, R. R., & Williams, A. M. (2007). The efficacy of demonstrations in teaching children an unfamiliar movement skill: the effects of object-orientated actions and point-light demonstrations. J Sports Sci, 25(5), 559-575.

Heyes, C. (2001). Causes and consequences of imitation. Trends Cogn Sci, 5(6), 253-261.

Heyes, C. M., & Foster, C. L. (2002). Motor learning by observation: evidence from a serial reaction time task. Quarterly Journal of Experimental Psychology Section A: Human Experimental Psychology, 55(2), 593-607.

Hickok, G., & Hauser, M. (2010). (Mis)understanding mirror neurons. Curr Biol, 20(14), R593-594.

Hodges, N. J., & Franks, I. M. (2000). Attention focusing instructions and coordination bias: implications for learning a novel bimanual task. Human Movement Science, 19, 843-867.

Hodges, N. J., & Williams, A. M. (2007). Current status of observational learning research and the role of demonstrations in sport. Journal Of Sports Sciences, 25(5), 495-496.

Hodges, N. J., Williams, A. M., Hayes, S. J., & Breslin, G. (2007). What is modelled during observational learning? Journal Of Sports Sciences, 25(5), 531-545.

Horn, R. R., Williams, A. M., Hayes, S. J., Hodges, N. J., & Scott, M. A. (2007). Demonstration as a rate enhancer to changes in coordination during early skill acquisition. Journal of Sports Sciences, 25(5), 599-614.

Horn, R. R., Williams, A. M., & Scott, M. A. (2002). Learning from demonstrations: the role of visual search during observational learning from video and point-light models. J Sports Sci, 20(3), 253-269.

Horn, R. R., Williams, A. M., Scott, M. A., & Hodges, N. J. (2005). Visual search and coordination changes in response to video and point-light demonstrations without KR. J Mot Behav, 37(4), 265-274.

Howard, I. S., Ingram, J. N., & Wolpert, D. M. (2011). Separate representations of dynamics in rhythmic and discrete movements: Evidence from motor learning. Journal of Neurophysiology, 105(4), 1722-1731.

Howatson, G, Zult T, Farthing J, Zijdwind I & Hortobágyi T (2013). Mirror training to augment interlimb transfer: A hypothesis. Frontiers in Human Neuroscience, 24;7:396. doi: 10.3389/fnhum.2013.00396, 2013.

Janelle, C. M., Champenoy, J. D., Coombes, S. A., & Mousseau, M. B. (2003). Mechanisms of attentional cueing during observational learning to facilitate motor skill acquisition. J Sports Sci, 21(10), 825-838.

Jeannerod, M. (2001). Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage, 14(1 Pt 2), S103-109.

Jeannerod, M. (2006). The origin of voluntary action: history of a physiological concept. Comptes Rendus Biologies, 329(5-6), 354-362.

Jeannerod, M., Arbib, M. A., Rizzolatti, G., & Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci, 18(7), 314-320.

Jordan, M. I. (1996) Chapter 2 Computational aspects of motor control and motor learning. Vol. 2. Handbook of Perception and Action (pp. 71-120).

Kilner, J. M. (2011). More than one pathway to action understanding. Trends Cogn Sci, 15(8), 352-357.

Kim, Y. T., Seo, J. H., Song, H. J., Yoo, D. S., Lee, H. J., Lee, J., . . . Chang, Y. (2011). Neural correlates related to action observation in expert archers. Behavioural Brain Research, 223(2), 342-347.

Knoblich, G., & Flach, R. (2001). Predicting the effects of actions: interactions of perception and action. Psychol Sci, 12(6), 467-472.

Koch, G., Versace, V., Bonni, S., Lupo, F., Gerfo, E. L., Oliveri, M., & Caltagirone, C. (2010). Resonance of cortico-cortical connections of the motor system with the observation of goal directed grasping movements. Neuropsychologia, 48(12), 3513-3520.

Króliczak, G., & Frey, S. H. (2009). A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cerebral Cortex, 19(10), 2396-2410.

Lago, A., & Fernandez-del-Olmo, M. (2011). Movement observation specifies motor programs activated by the action observed objective. Neurosci Lett, 493(3), 102-106.

Lago, A., Koch, G., Cheeran, B., Marquez, G., Sanchez, J. A., Ezquerro, M., . . . Fernandez-del-Olmo, M. (2010). Ventral premotor to primary motor cortical interactions during noxious and naturalistic action observation. Neuropsychologia, 48(6), 1802-1806.

Lago-Rodriguez, A., Lopez-Alonso, V., & Fernandez-del-Olmo, M. (2013). Mirror neuron system and observational learning: Behavioral and neurophysiological evidence. Behavioural Brain Research, 248, 104-113.

Land, M. F., & McLeod, P. (2000). From eye movements to actions: Batsmen hit the ball. Nature Neuroscience, 3(12), 1340-1345.

Lepage, J. F., Tremblay, S., & Theoret, H. (2010). Early non-specific modulation of corticospinal excitability during action observation. Eur J Neurosci, 31(5), 931-937.

Liepelt, R., Prinz, W., & Brass, M. (2010). When do we simulate non-human agents? Dissociating communicative and non-communicative actions. Cognition, 115(3), 426-434.

Logothetis, N. K. (2008). What we can do and what we cannot do with fMRI. Nature, 453(7197), 869-878.

Mann, D. L., Abernethy, B., & Farrow, D. (2010). Action specificity increases anticipatory performance and the expert advantage in natural interceptive tasks. Acta Psychologica, 135(1), 17-23.

Maslovat, D., Hodges, N. J., Krigolson, O. E., & Handy, T. C. (2010). Observational practice benefits are limited to perceptual improvements in the acquisition of a novel coordination skill. Experimental Brain Research, 204(1), 119-130.

McCullagh, P., & Meyer, K. N. (1997). Learning versus correct models: influence of model type on the learning of a free-weight squat lift. Research Quarterly For Exercise And Sport, 68(1), 56-61.

McCullagh, P., & Weiss, M. R. (2001). Modeling: considerations for motor skill performance and psychological responses. Handbook of sport psychology, 205-238.

Miall, R. C. (2003). Connecting mirror neurons and forward models. Neuroreport, 14(17), 2135-2137.

Miall, R. C., Stanley, J., Todhunter, S., Levick, C., Lindo, S., & Miall, J. D. (2006). Performing hand actions assists the visual discrimination of similar hand postures. Neuropsychologia, 44(6), 966-976.

Miall, R. C., & Wolpert, D. M. (1996). Forward models for physiological motor control. Neural Networks, 9(8), 1265-1279.

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(1), 341-349.

Montagna, M., Cerri, G., Borroni, P., & Baldissera, F. (2005). Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action. Eur J Neurosci, 22(6), 1513-1520.

Mukamel, R., Ekstrom, A. D., Kaplan, J., Iacoboni, M., & Fried, I. (2010). Single-neuron responses in humans during execution and observation of actions. Curr Biol, 20(8), 750-756.

Müller, S., Abernethy, B., & Farrow, D. (2006). How do world-class cricket batsmen anticipate a bowler's intention? Quarterly Journal of Experimental Psychology, 59(12), 2162-2186.

Nojima I, Mima T, Koganemaru S, Thabit MN, Fukuyama H & Kawamata T (2012) .Human motor plasticity induced by mirror visual feedback. J Neurosci, 32(4),1293-300.

Press, C., Bird, G., Walsh, E., & Heyes, C. (2008). Automatic imitation of intransitive actions. Brain and Cognition, 67(1), 44-50.

Prinz, W. (1997). Perception and Action Planning. European journal of cognitive psychology, 9, 129-154.

Prinz, W., & Hommel, B. (2002). Common mechanisms in perception and action. In W. Prinz & B. Hommel (Eds.), Attention and performance (1st ed ed., Vol. XIX). Oxford: Oxford University Press.

Ram, N., Riggs, S. M., Skaling, S., Landers, D. M., & McCullagh, P. (2007). A comparison of modelling and imagery in the acquisition and retention of motor skills. J Sports Sci, 25(5), 587-597.

Rizzolatti, G., Cattaneo, L., Fabbri-Destro, M., & Rozzi, S. (2014). Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiological Reviews, 94(2), 655-706.

Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annu Rev Neurosci, 27, 169-192.

Rizzolatti, G., & Fogassi, L. (2014). The mirror mechanism: Recent findings and perspectives. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1644).

Rizzolatti, G., Luppino, G., & Matelli, M. (1998). The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol, 106(4), 283-296.

Rizzolatti, G., & Sinigaglia, C. (2010). The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci, 11(4), 264-274.

Rohbanfard, H., & Proteau, L. (2011). Learning through observation: A combination of expert and novice models favors learning. Experimental Brain Research, 215(3-4), 183-197.

Romani, M., Cesari, P., Urgesi, C., Facchini, S., & Aglioti, S. M. (2005). Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements. Neuroimage, 26(3), 755-763.

Rossi, S., Hallett, M., Rossini, P. M., Pascual-Leone, A., Avanzini, G., Bestmann, S., Ziemann, U. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120(12), 2008-2039.

Sakamoto, M., Muraoka, T., Mizuguchi, N., & Kanosue, K. (2009). Execution-dependent modulation of corticospinal excitability during action observation. Exp Brain Res, 199(1), 17-25.

Sanchez-Ku, M. L., & Arthur W, Jr. (2000). A dyadic protocol for training complex skills: A replication using female participants. Human Factors, 42(3), 512-520.

Savelsbergh, G. J., Williams, A. M., Van der Kamp, J., & Ward, P. (2002). Visual search, anticipation and expertise in soccer goalkeepers. J Sports Sci, 20(3), 279-287.

Schubo, A., Prinz, W., & Aschersleben, G. (2004). Perceiving while acting: action affects perception. Psychol Res, 68(4), 208-215.

Schutz-Bosbach, S., & Prinz, W. (2007). Perceptual resonance: action-induced modulation of perception. Trends Cogn Sci, 11(8), 349-355.

Senna, I., Bolognini, N., & Maravita, A. (2014). Grasping with the foot: Goal and motor expertise in action observation. Human Brain Mapping, 35(4), 1750-1760.

Shea, C. H., Wulf, G., & Whitacre, C. (1999). Enhancing Training Efficiency and Effectiveness Through the Use of Dyad Training. J Mot Behav, 31(2), 119-125.

Shebilske, W. L., Regian, J. W., Arthur Jr, W., & Jordan, J. A. (1992). A dyadic protocol for training complex skills. Human Factors, 34(3), 369-374.

Sheffield, F. D. (1961). Theoretical consideration in the learning of complex sequential task from demonstration and practice. Student Response in Programmed Instruction, 13-32.

Spilka, M. J., Steele, C. J., & Penhune, V. B. (2010). Gesture imitation in musicians and non-musicians. Exp Brain Res, 204(4), 549-558.

Starkes, J. L., Edwards, P., Dissanayake, P., & Dunn, T. (1995). A new technology and field test of advance cue usage in volleyball. Research Quarterly For Exercise And Sport, 66(2), 162-167.

Stoet, G., & Hommel, B. (2002). Interactions between feature binding in perception and action. In W. Prinz & B. Hommel (Eds.), Common mechanisms in perception and action (Attention and Performance) (Vol. XIX). Oxford: Oxford University Press.

Strafella, A. P., & Paus, T. (2000). Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport, 11(10), 2289-2292.

Viviani, P., & Stucchi, N. (1992). Biological movements look uniform: evidence of motor-perceptual interactions. Journal of Experimental Psychology: Human Perception and Performance, 18(3), 603-623.

Vogt, S. (2002). Visuomotor couplings in object-oriented and imitative actions. In A. N. Meltzoff & W. Prinz (Eds.), The imitative mind: Development, evolution, and brain bases (pp. 206-220). Cambridge: Cambridge University Press.

Vogt, S., & Thomaschke, R. (2007). From visuo-motor interactions to imitation learning: behavioural and brain imaging studies. Journal Of Sports Sciences, 25(5), 497-517.

Walsh, V., & Rushworth, M. (1999). A primer of magnetic stimulation as a tool for neuropsychology. Neuropsychologia, 37(2), 125-135.

Weeks, D. L., & Anderson, L. P. (2000). The interaction of observational learning with overt practice: effects on motor skill learning. Acta Psychol (Amst), 104(2), 259-271.

Williams, A. M., Ward, P., Knowles, J. M., & Smeeton, N. J. (2002). Anticipation skill in a real-world task: measurement, training, and transfer in tennis. J Exp Psychol Appl, 8(4), 259-270.

Wolpert, D. M. (1997). Computational approaches to motor control. Trends in Cognitive Sciences, 1(6), 209-216.

Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science, 269(5232), 1880-1882.

Wolpert, D. M., Miall, R. C., & Kawato, M. (1998). Internal models in the cerebellum. Trends in Cognitive Sciences, 2(9), 338-347.

Wulf, G., Shea, C., & Lewthwaite, R. (2010). Motor skill learning and performance: a review of influential factors. Med Educ, 44(1), 75-84.

Yarrow, K., Brown, P., & Krakauer, J. W. (2009). Inside the brain of an elite athlete: The neural processes that support high achievement in sports. Nature Reviews Neuroscience, 10(8), 585-596.

Ziemann, U., Lonnecker, S., Steinhoff, B. J., & Paulus, W. (1996). Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol, 40(3), 367-378.

Zwickel, J., Grosjean, M., & Prinz, W. (2007). Seeing while moving: measuring the online influence of action on perception. Q J Exp Psychol (Hove), 60(8), 1063-1071.

Zult T, Howatson G, Kádár E, Farthing J & Hortobágyi T (2014). Role of the mirror neuron system in cross-education. Sports Medicine, 44,159-178.

Downloads

Published

2014-07-11

Issue

Section

Original Research

Most read articles by the same author(s)