Review
Where do mirror neurons come from?

https://doi.org/10.1016/j.neubiorev.2009.11.007Get rights and content

Abstract

Debates about the evolution of the ‘mirror neuron system’ imply that it is an adaptation for action understanding. Alternatively, mirror neurons may be a byproduct of associative learning. Here I argue that the adaptation and associative hypotheses both offer plausible accounts of the origin of mirror neurons, but the associative hypothesis has three advantages. First, it provides a straightforward, testable explanation for the differences between monkeys and humans that have led some researchers to question the existence of a mirror neuron system. Second, it is consistent with emerging evidence that mirror neurons contribute to a range of social cognitive functions, but do not play a dominant, specialised role in action understanding. Finally, the associative hypothesis is supported by recent data showing that, even in adulthood, the mirror neuron system can be transformed by sensorimotor learning. The associative account implies that mirror neurons come from sensorimotor experience, and that much of this experience is obtained through interaction with others. Therefore, if the associative account is correct, the mirror neuron system is a product, as well as a process, of social interaction.

Section snippets

Properties of mirror neurons in monkeys

Matching is the most basic property of mirror neurons—they fire when the monkey observes and performs similar actions. The adaptation hypothesis explains this matching in terms of the putative function of mirror neurons (see Table 1): the evolution of neurons that respond during observation and execution of similar actions has been favoured by natural selection because, in contrast with, for example, neurons that fire when one action is observed and different action is executed, they enable the

Is there a human ‘mirror neuron system’?

Research using transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) has been interpreted by many researchers as evidence that humans also have mirror neurons or, more broadly, a ‘mirror neuron system’. TMS studies show that passive observation of arm, hand and finger movements results in selective activation of the muscles involved in producing the observed movement (Aziz-Zadeh et al., 2002, Catmur et al., 2007, Fadiga et al., 1995, Gangitano et al., 2001,

Imitation in newborns?

Newborn infants have had minimal opportunity for sensorimotor learning. Therefore evidence of mirror neuron system activity in newborn monkeys or humans would provide strong support for the adaptation hypothesis over the associative hypothesis (Meltzoff and Decety, 2003, Rizzolatti et al., 2002). No direct evidence of this kind is available. However, it has been argued that imitation depends on the mirror neuron system, and therefore that studies reporting imitation in neonates provide indirect

Conclusions and future directions

The associative hypothesis could be tested more decisively by examining the effects of incompatible sensorimotor experience on mirror neurons in monkeys. This hypothesis predicts that if monkeys were given experience in which, for example, observation of a precision grip is reliably correlated with execution of a power grip, then some of the mirror neurons that were previously responsive to observation and execution of a precision grip would become counter-mirror neurons, discharging during

Acknowledgements

I am grateful to Geoff Bird, Charlotte Bonardi, Marcel Brass, Caroline Catmur, Richard Cook, Anthony Dickinson, Martin Eimer, Chris Frith, James Kilner, Dick Passingham, Matthew Rushworth, Clare Press, Elizabeth Ray, Sophie Scott, David Shanks and Nick Shea for their help and encouragement. I would also like to thank Steve Duxbury, Julia and Lily Fogerty, Mary Heyes, and the children of St Teresa's Catholic Primary School, Ashford, for their help with Fig. 1.

References (100)

  • V. Gazzola et al.

    The anthropomorphic brain: the mirror neuron system responds to human and robotic actions

    Neuroimage

    (2007)
  • J. Grèzes et al.

    Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study

    Neuroimage

    (2003)
  • G. Hall

    Pavlovian conditioning: laws of association

  • C. Heyes et al.

    Experience modulates automatic imitation

    Cognitive Brain Research

    (2005)
  • C.M. Heyes et al.

    What is the significance of imitation in animals?

    Advances in the Study of Behavior

    (2000)
  • M. Jonas

    Do simple intransitive finger movements consistently activate frontoparietal mirror neuron areas in humans?

    Neuroimage

    (2007)
  • C. Keysers et al.

    Demystifying social cognition: a Hebbian perspective

    Trends in Cognitive Sciences

    (2004)
  • E.M. MacPhail

    Cognitive function in mammals: the evolutionary perspective

    Cognitive Brain Research

    (1996)
  • B.Z. Mahon et al.

    A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content

    Journal of Physiology

    (2008)
  • G. Rizzolatti et al.

    Language within our grasp

    Trends in Neurosciences

    (1998)
  • G. Rizzolatti et al.

    Premotor cortex and the recognition of motor actions

    Cognitive Brain Research

    (1996)
  • M.A. Umilta

    I know what you are doing: a neurophysiological study

    Neuron

    (2001)
  • S. Vogt

    Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise

    Neuroimage

    (2007)
  • L. Aziz-Zadeh et al.

    Lateralization of the human mirror neuron system

    Journal of Neuroscience

    (2006)
  • L. Aziz-Zadeh et al.

    Lateralization in motor facilitation during action observation: a TMS study

    Experimental Brain Research

    (2002)
  • Blakeslee, S., 2006. Cells that read minds. The New York Times, January 10....
  • C. Bonardi

    Conditional learning: an associative analysis

  • G. Buccino

    Neural circuits involved in the recognition of actions performed by nonconspecifics: an fMRI study

    Journal of Cognitive Neuroscience

    (2004)
  • B. Calvo-Merino et al.

    Action observation and acquired motor skills: an fMRI study with expert dancers

    Cerebral Cortex

    (2005)
  • C. Catmur et al.

    Through the looking glass: counter-mirror activation following incompatible sensorimotor learning

    European Journal of Neuroscience

    (2008)
  • Catmur, C., Mars, R., Rushworth, M., Heyes, C.M., in press. Making mirrors: premotor cortex stimulation enhances mirror...
  • C. Catmur et al.

    Associative sequence learning: the role of experience in the development of imitation and the mirror system

    Philosophical Transactions of the Royal Society B

    (2009)
  • T. Chaminade

    From mirror neurons to human cognition: the missing links

  • Cook, R., Press, C., Heyes, C.M., in press. Is the acquisition of automatic imitation sensitive to sensorimotor...
  • A. D’Ausilio et al.

    Cross-modal plasticity of the motor cortex while listening to a rehearsed musical piece

    European Journal of Neuroscience

    (2006)
  • M. Del Giudice et al.

    Programmed to learn? The ontogeny of mirror neurons

    Developmental Science

    (2009)
  • I. Dinstein et al.

    A mirror up to nature

    Current Biology

    (2008)
  • I. Dinstein et al.

    Brain areas selective for both observed and executed movements

    Journal of Neurophysiology

    (2007)
  • G. Di Pellegrino et al.

    Understanding motor events: a neurophysiological study

    Experimental Brain Research

    (1992)
  • L. Fadiga et al.

    Motor facilitation during action observation: a magnetic stimulation study

    Journal of Neurophysiology

    (1995)
  • P.F. Ferrari et al.

    Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex

    European Journal of Neuroscience

    (2003)
  • P.F. Ferrari et al.

    Mirror neuron responding to observation of actions made with tools in monkey ventral premotor cortex

    Journal of Cognitive Neuroscience

    (2005)
  • P.F. Ferrari

    Neonatal imitation in rhesus macaques

    PLoS Biology

    (2006)
  • L. Fogassi et al.

    Parietal lobe: from action organization to intention understanding

    Science

    (2005)
  • V. Gallese et al.

    Action recognition in the premotor cortex

    Brain

    (1996)
  • V. Gallese et al.

    Action representation and the inferior parietal lobule

  • V. Gallese et al.

    Mirror neurons and the simulation theory of mind-reading

    Trends in Cognitive Sciences

    (1998)
  • M. Gangitano et al.

    Phase-specific modulation of cortical motor output during movement observation

    Neuroreport

    (2001)
  • M. Gangitano et al.

    Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements

    European Journal of Neuroscience

    (2004)
  • V. Gazzola et al.

    The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data

    Cerebral Cortex

    (2009)
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