Predictive motor activation during action observation in human infants

Certain regions of the human brain are activated both during action execution and action observation. This so-called ‘mirror neuron system’ has been proposed to enable an observer to understand an action through a process of internal motor simulation. Although there has been much speculation about the existence of such a system from early in life, to date there is little direct evidence that young infants recruit brain areas involved in action production during action observation. To address this question, we identified the individual frequency range in which sensorimotor alpha-band activity was attenuated in nine-month-old infants' electroencephalographs (EEGs) during elicited reaching for objects, and measured whether activity in this frequency range was also modulated by observing others' actions. We found that observing a grasping action resulted in motor activation in the infant brain, but that this activity began prior to observation of the action, once it could be anticipated. These results demonstrate not only that infants, like adults, display overlapping neural activity during execution and observation of actions, but that this activation, rather than being directly induced by the visual input, is driven by infants' understanding of a forthcoming action. These results provide support for theories implicating the motor system in action prediction.

[1]  Ruth M. Cruikshank The Development of Visual Size Constancy in Early Infancy , 1941 .

[2]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[3]  Victoria Southgate,et al.  Inferring the outcome of an ongoing novel action at 13 months. , 2009, Developmental psychology.

[4]  G. Csibra Action mirroring and action understanding: an alternative account , 1993 .

[5]  R. Passingham,et al.  Action observation and acquired motor skills: an FMRI study with expert dancers. , 2005, Cerebral cortex.

[6]  Hein T. van Schie,et al.  You'll never crawl alone: Neurophysiological evidence for experience-dependent motor resonance in infancy , 2008, NeuroImage.

[7]  T. Mergner,et al.  Selecting relevant electrode positions for classification tasks based on the electro-encephalogram , 2006, Medical and Biological Engineering and Computing.

[8]  A. Woodward Infants' ability to distinguish between purposeful and non-purposeful behaviors , 1999 .

[9]  Sarah-Jayne Blakemore,et al.  How does the mirror neuron system change during development? , 2007, Developmental science.

[10]  H. Théoret,et al.  EEG evidence for the presence of an action observation–execution matching system in children , 2006, The European journal of neuroscience.

[11]  Pär Nyström,et al.  The infant mirror neuron system studied with high density EEG , 2008, Social neuroscience.

[12]  Kazuo Hiraki,et al.  Infant's brain responses to live and televised action , 2006, NeuroImage.

[13]  S. Blakemore,et al.  Motor activation prior to observation of a predicted movement , 2004, Nature Neuroscience.

[14]  G. Rizzolatti,et al.  The mirror neuron system. , 2009, Archives of neurology.

[15]  G. Rizzolatti,et al.  Activation of human primary motor cortex during action observation: a neuromagnetic study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Hari,et al.  Human cortical oscillations: a neuromagnetic view through the skull , 1997, Trends in Neurosciences.

[17]  C. Frith,et al.  Relationship between Activity in Human Primary Motor Cortex during Action Observation and the Mirror Neuron System , 2009, PloS one.

[18]  A Step Forward for Mirror Neurons? Investigating the Functional Link between Action Execution and Action Observation in Limb Apraxia , 2008, The Journal of Neuroscience.

[19]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[20]  Riitta Hari,et al.  Actor's and observer's primary motor cortices stabilize similarly after seen or heard motor actions , 2007, Proceedings of the National Academy of Sciences.

[21]  Gregory Hickok,et al.  Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans , 2009, Journal of Cognitive Neuroscience.