Dynamic Modulation of Human Motor Activity When Observing Actions

Previous studies have demonstrated that when we observe somebody else executing an action many areas of our own motor systems are active. It has been argued that these motor activations are evidence that we motorically simulate observed actions; this motoric simulation may support various functions such as imitation and action understanding. However, whether motoric simulation is indeed the function of motor activations during action observation is controversial, due to inconsistency in findings. Previous studies have demonstrated dynamic modulations in motor activity when we execute actions. Therefore, if we do motorically simulate observed actions, our motor systems should also be modulated dynamically, and in a corresponding fashion, during action observation. Using magnetoencephalography, we recorded the cortical activity of human participants while they observed actions performed by another person. Here, we show that activity in the human motor system is indeed modulated dynamically during action observation. The finding that activity in the motor system is modulated dynamically when observing actions can explain why studies of action observation using functional magnetic resonance imaging have reported conflicting results, and is consistent with the hypothesis that we motorically simulate observed actions.

[1]  P. Viviani,et al.  The law relating the kinematic and figural aspects of drawing movements. , 1983, Acta psychologica.

[2]  K. Hollis,et al.  The biological function of Pavlovian conditioning: the best defense is a good offense. , 1984, Journal of experimental psychology. Animal behavior processes.

[3]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[4]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[6]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[7]  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.

[8]  S. Cochin,et al.  Perception of motion and qEEG activity in human adults. , 1998, Electroencephalography and clinical neurophysiology.

[9]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[10]  S. Cochin,et al.  Observation and execution of movement: similarities demonstrated by quantified electroencephalography , 1999, The European journal of neuroscience.

[11]  V. Gallese Action representaion and the inferior parietal lobule , 2000 .

[12]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[13]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[14]  A. Schnitzler,et al.  Dynamic imaging of coherent sources: Studying neural interactions in the human brain. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  G. Rizzolatti,et al.  I Know What You Are Doing A Neurophysiological Study , 2001, Neuron.

[16]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

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

[18]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[19]  Febo Cincotti,et al.  Human Cortical Electroencephalography (EEG) Rhythms during the Observation of Simple Aimless Movements: A High-Resolution EEG Study , 2002, NeuroImage.

[20]  K. Doya,et al.  A unifying computational framework for motor control and social interaction. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  R. Miall,et al.  Connecting mirror neurons and forward models. , 2003, Neuroreport.

[22]  Riitta Hari,et al.  Task-Dependent Modulations of Cortical Oscillatory Activity in Human Subjects during a Bimanual Precision Grip Task , 2003, NeuroImage.

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

[24]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

[25]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[26]  D. Perrett,et al.  Opinion TRENDS in Cognitive Sciences Vol.8 No.11 November 2004 Demystifying social cognition: a Hebbian perspective , 2022 .

[27]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

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

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

[30]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[31]  Geoffrey Bird,et al.  Effector-dependent learning by observation of a finger movement sequence. , 2005, Journal of experimental psychology. Human perception and performance.

[32]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

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

[34]  Talma Hendler,et al.  Neural representations of kinematic laws of motion: Evidence for action-perception coupling , 2007, Proceedings of the National Academy of Sciences.

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

[36]  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.

[37]  Karl J. Friston,et al.  The mirror-neuron system: a Bayesian perspective. , 2007, Neuroreport.

[38]  Karl J. Friston,et al.  Predictive coding: an account of the mirror neuron system , 2007, Cognitive Processing.

[39]  A. Hamilton,et al.  Interference effect of observed human movement on action is due to velocity profile of biological motion , 2007, Social neuroscience.

[40]  Eran Stark,et al.  Distinct movement parameters are represented by different neurons in the motor cortex , 2007, The European journal of neuroscience.

[41]  David J. Heeger,et al.  A mirror up to nature , 2008 .

[42]  J. Grèzes,et al.  What is “mirror” in the premotor cortex? A review , 2008, Neurophysiologie Clinique/Clinical Neurophysiology.

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

[44]  Alfonso Caramazza,et al.  Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans , 2009, Proceedings of the National Academy of Sciences.

[45]  C. Keysers,et al.  The Observation and Execution of Actions Share Motor and Somatosensory Voxels in all Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data , 2008, Cerebral cortex.

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

[47]  R. Vogels,et al.  Functional differentiation of macaque visual temporal cortical neurons using a parametric action space. , 2009, Cerebral cortex.

[48]  T. Flash,et al.  Neuronal encoding of human kinematic invariants during action observation. , 2010, Cerebral cortex.

[49]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[50]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[51]  Juliana Dushanova,et al.  Neurons in primary motor cortex engaged during action observation , 2010, The European journal of neuroscience.

[52]  C. Heyes Where do mirror neurons come from? , 2010, Neuroscience & Biobehavioral Reviews.

[53]  Karl J. Friston,et al.  Topological inference for EEG and MEG , 2010, 1011.2901.

[54]  Anne Springer,et al.  Predicting and memorizing observed action: Differential premotor cortex involvement , 2011, Human brain mapping.