Timecourse of mirror and counter-mirror effects measured with transcranial magnetic stimulation

The human mirror system has been the subject of much research over the past two decades, but little is known about the timecourse of mirror responses. In addition, it is unclear whether mirror and counter-mirror effects follow the same timecourse. We used single-pulse transcranial magnetic stimulation to investigate the timecourse of mirror and counter-mirror responses in the human brain. Experiment 1 demonstrated that mirror responses can be measured from around 200 ms after observed action onset. Experiment 2 demonstrated significant effects of counter-mirror sensorimotor training at all timepoints at which a mirror response was found in Experiment 1 (i.e. from 200 ms onward), indicating that mirror and counter-mirror responses follow the same timecourse. By suggesting similarly direct routes for mirror and counter-mirror responses, these results support the associative account of mirror neuron origins whereby mirror responses arise as a result of correlated sensorimotor experience during development. More generally, they contribute to theorizing regarding mirror neuron function by providing some constraints on how quickly mirror responses can influence social cognition.

[1]  H. Théoret,et al.  Early non‐specific modulation of corticospinal excitability during action observation , 2010, The European journal of neuroscience.

[2]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[3]  B. Gandevia,et al.  DECLARATION OF HELSINKI. , 1964, The Medical journal of Australia.

[4]  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.

[5]  C. Heyes,et al.  Experience modulates automatic imitation. , 2005, Brain research. Cognitive brain research.

[6]  Maria Alessandra Umiltà,et al.  Responses of mirror neurons in area F5 to hand and tool grasping observation , 2010, Experimental Brain Research.

[7]  L. Fogassi,et al.  Audiovisual mirror neurons and action recognition , 2003, Experimental Brain Research.

[8]  Paul E. Downing,et al.  Learning associations between action and perception: Effects of incompatible training on body part and spatial priming , 2011, Brain and Cognition.

[9]  G. Rizzolatti,et al.  View-Based Encoding of Actions in Mirror Neurons of Area F5 in Macaque Premotor Cortex , 2011, Current Biology.

[10]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[11]  R. Hari,et al.  Temporal dynamics of cortical representation for action. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Catmur.  Sensorimotor learning and the ontogeny of the mirror neuron system , 2013, Neuroscience Letters.

[13]  Á. Pascual-Leone,et al.  Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements , 2004, The European journal of neuroscience.

[14]  Luigi Cattaneo,et al.  Early and late motor responses to action observation. , 2013, Social cognitive and affective neuroscience.

[15]  T. Paus,et al.  Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study , 2000, Neuroreport.

[16]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

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

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

[19]  Giuseppe Riva,et al.  Mirroring avatars: dissociation of action and intention in human motor resonance , 2011, The European journal of neuroscience.

[20]  Paul E. Downing,et al.  Viewpoint (In)dependence of Action Representations: An MVPA Study , 2012, Journal of Cognitive Neuroscience.

[21]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[22]  Luciano Fadiga,et al.  Force requirements of observed object lifting are encoded by the observer’s motor system: a TMS study , 2010, The European journal of neuroscience.

[23]  E. Wassermann.  Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

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

[25]  S. Eckstein.  Ethical principles for medical research involving human subjects. , 2001, European journal of emergency medicine : official journal of the European Society for Emergency Medicine.

[26]  Caroline Catmur,et al.  Making Mirrors: Premotor Cortex Stimulation Enhances Mirror and Counter-mirror Motor Facilitation , 2011, Journal of Cognitive Neuroscience.

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

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

[29]  Francesca Ugolotti Serventi,et al.  Ventral premotor and inferior parietal cortices make distinct contribution to action organization and intention understanding. , 2010, Cerebral cortex.

[30]  World Medical Association (WMA),et al.  Declaration of Helsinki. Ethical Principles for Medical Research Involving Human Subjects , 2009, Journal of the Indian Medical Association.

[31]  Lee Hoong-Chien,et al.  Supplementary Table 4 , 2015 .

[32]  R. Oostenveld,et al.  Evidence for fast, low-level motor resonance to action observation: An MEG study , 2008, Social neuroscience.

[33]  S. Chandrasekharan,et al.  Activity of human motor system during action observation is modulated by object presence , 2011, Experimental Brain Research.

[34]  Cecilia Heyes,et al.  Action Preparation Helps and Hinders Perception of Action , 2010, Journal of Cognitive Neuroscience.

[35]  Leslie G. Ungerleider,et al.  Formation of a Motor Memory by Action Observation , 2005, The Journal of Neuroscience.

[36]  Marcel Brass,et al.  Experience-based priming of body parts: A study of action imitation , 2008, Brain Research.

[37]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

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

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

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

[41]  Cecilia Heyes,et al.  Acquisition of automatic imitation is sensitive to sensorimotor contingency. , 2010, Journal of experimental psychology. Human perception and performance.

[42]  Alison J. Wiggett,et al.  Surface-Based Information Mapping Reveals Crossmodal Vision–Action Representations in Human Parietal and Occipitotemporal Cortex , 2010, Journal of neurophysiology.

[43]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[44]  Christian Keysers,et al.  Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data , 2008, PloS one.

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

[46]  Alexander Kraskov,et al.  Corticospinal Neurons in Macaque Ventral Premotor Cortex with Mirror Properties: A Potential Mechanism for Action Suppression? , 2009, Neuron.

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

[48]  Caroline Catmur,et al.  Sensorimotor Learning Configures the Human Mirror System , 2007, Current Biology.

[49]  A. Dickinson,et al.  Contextual modulation of mirror and countermirror sensorimotor associations. , 2012, Journal of experimental psychology. General.

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

[51]  Á. Pascual-Leone,et al.  Phase-specific modulation of cortical motor output during movement observation , 2001, Neuroreport.

[52]  V. Ramachandran,et al.  The human mirror neuron system: a link between action observation and social skills. , 2007, Social cognitive and affective neuroscience.

[53]  John R. Williams.  DECLARATION OF HELSINKI , 1964 .

[54]  Marcel Brass,et al.  Through the looking glass: counter‐mirror activation following incompatible sensorimotor learning , 2008, The European journal of neuroscience.

[55]  J. R. Simon,et al.  Reactions toward the source of stimulation. , 1969, Journal of experimental psychology.

[56]  Gabriella Cerri,et al.  Bilateral motor resonance evoked by observation of a one‐hand movement: role of the primary motor cortex , 2008, The European journal of neuroscience.