Virtual Lesions of the IFG Abolish Response Facilitation for Biological and Non-Biological Cues

Humans are faster to perform a given action following observation of that same action. Converging evidence suggests that the human mirror neuron system (MNS) plays an important role in this phenomenon. However, the specificity of the neural mechanisms governing this effect remain controversial. Specialist theories of imitation suggest that biological cues are maximally capable of eliciting imitative facilitation. Generalist models, on the other hand, posit a broader role for the MNS in linking visual stimuli with appropriate responses. In the present study, we investigated the validity of these two theoretical approaches by disrupting the left and right inferior frontal gyrus (IFG) during the preparation of congruent (imitative) and incongruent (complementary) actions cued by either biological (hand) or non-biological (static dot) stimuli. Delivery of TMS over IFG abolished imitative response facilitation. Critically, this effect was identical whether actions were cued by biological or non-biological stimuli. This finding argues against theories of imitation in which biological stimuli are treated preferentially and stresses the notion of the IFG as a vital center of general perception–action coupling in the human brain.

[1]  Karl J. Friston,et al.  Evidence of Mirror Neurons in Human Inferior Frontal Gyrus , 2009, The Journal of Neuroscience.

[2]  Marcel Brass,et al.  Neural Correlates of Overcoming Interference from Instructed and Implemented Stimulus–Response Associations , 2009, The Journal of Neuroscience.

[3]  H. Bekkering,et al.  Understanding action beyond imitation: reversed compatibility effects of action observation in imitation and joint action. , 2008, Journal of experimental psychology. Human perception and performance.

[4]  Marcel Brass,et al.  What is matched in direct matching? Intention attribution modulates motor priming. , 2008, Journal of experimental psychology. Human perception and performance.

[5]  C. Heyes,et al.  Stimulus-driven selection of routes to imitation , 2008, Experimental Brain Research.

[6]  Scott T. Grafton,et al.  Action outcomes are represented in human inferior frontoparietal cortex. , 2008, Cerebral cortex.

[7]  S. Hurley The shared circuits model (SCM): how control, mirroring, and simulation can enable imitation, deliberation, and mindreading. , 2008, The Behavioral and brain sciences.

[8]  A. Schnitzler,et al.  Do simple intransitive finger movements consistently activate frontoparietal mirror neuron areas in humans? , 2007, NeuroImage.

[9]  H. Bekkering,et al.  The mirror neuron system is more active during complementary compared with imitative action , 2007, Nature Neuroscience.

[10]  Andrew D. Wilson,et al.  Methodological problems undermine tests of the ideo-motor conjecture , 2007, Experimental Brain Research.

[11]  Christian Keysers,et al.  The anthropomorphic brain: The mirror neuron system responds to human and robotic actions , 2007, NeuroImage.

[12]  Alexander Münchau,et al.  Investigating the human mirror neuron system by means of cortical synchronization during the imitation of biological movements , 2006, NeuroImage.

[13]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[14]  J. Mazziotta,et al.  Lateralization of the Human Mirror Neuron System , 2006, The Journal of Neuroscience.

[15]  Antonia F. de C. Hamilton,et al.  Action Understanding Requires the Left Inferior Frontal Cortex , 2006, Current Biology.

[16]  M. Brass,et al.  The inhibition of imitative and overlearned responses: a functional double dissociation , 2005, Neuropsychologia.

[17]  C. Heyes,et al.  Robotic movement elicits automatic imitation. , 2005, Brain research. Cognitive brain research.

[18]  M. Brass,et al.  Imitation: is cognitive neuroscience solving the correspondence problem? , 2005, Trends in Cognitive Sciences.

[19]  J. Mazziotta,et al.  Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. , 2005, Cerebral cortex.

[20]  M. Makuuchi Is Broca's area crucial for imitation? , 2005, Cerebral cortex.

[21]  R. Goebel,et al.  The Dynamics of Interhemispheric Compensatory Processes in Mental Imagery , 2005, Science.

[22]  M. Jeannerod,et al.  The motor theory of social cognition: a critique , 2005, Trends in Cognitive Sciences.

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

[24]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[25]  U. Castiello,et al.  The Human Premotor Cortex Is 'Mirror' Only for Biological Actions , 2004, Current Biology.

[26]  Y. Paulignan,et al.  An Interference Effect of Observed Biological Movement on Action , 2003, Current Biology.

[27]  J. Mazziotta,et al.  The essential role of Broca's area in imitation , 2003, The European journal of neuroscience.

[28]  Luciano Fadiga,et al.  Hand action preparation influences the responses to hand pictures , 2002, Neuropsychologia.

[29]  N. A. Borghese,et al.  Different Brain Correlates for Watching Real and Virtual Hand Actions , 2001, NeuroImage.

[30]  C. Heyes Causes and consequences of imitation , 2001, Trends in Cognitive Sciences.

[31]  J. Ashe,et al.  The Effect of Stimulus–Response Compatibility on Cortical Motor Activation , 2001, NeuroImage.

[32]  W. Prinz,et al.  Movement observation affects movement execution in a simple response task. , 2001, Acta psychologica.

[33]  G Aschersleben,et al.  Correspondence effects with manual gestures and postures: a study of imitation. , 2000, Journal of experimental psychology. Human perception and performance.

[34]  W. Prinz,et al.  Compatibility between Observed and Executed Finger Movements: Comparing Symbolic, Spatial, and Imitative Cues , 2000, Brain and Cognition.

[35]  M. Shiffrar,et al.  New aspects of motion perception: selective neural encoding of apparent human movements , 2000, Neuroreport.

[36]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[37]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[38]  A. Meltzoff,et al.  Imitation of Facial and Manual Gestures by Human Neonates , 1977, Science.

[39]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.