Anticipatory planning reveals segmentation of cortical motor output during action observation.

It has been argued that the variation in brain activity that occurs when observing another person reflects a representation of actions that is indivisible, and which plays out in full once the intent of the actor can be discerned. We used transcranial magnetic stimulation to probe the excitability of corticospinal projections to 2 intrinsic hand muscles while motions to reach and grasp an object were observed. A symbolic cue either faithfully indicated the required final orientation of the object and thus the nature of the grasp that was required, or was in conflict with the movement subsequently displayed. When the cue was veridical, modulation of excitability was in accordance with the functional role of the muscles in the action observed. If however the cue had indicated that the alternative grasp would be required, modulation of output to first dorsal interosseus was consistent with the action specified, rather than the action observed--until the terminal phase of the motion sequence during which the object was seen lifted. Modulation of corticospinal output during observation is thus segmented--it progresses initially in accordance with the action anticipated, and if discrepancies are revealed by visual input, coincides thereafter with that of the action seen.

[1]  Cosimo Urgesi,et al.  Compensatory plasticity in the action observation network: virtual lesions of STS enhance anticipatory simulation of seen actions. , 2013, Cerebral cortex.

[2]  C. Urgesi,et al.  Simulating the future of actions in the human corticospinal system. , 2010, Cerebral cortex.

[3]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

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

[5]  U. Castiello.  The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[6]  S. Small,et al.  The mirror neuron system and treatment of stroke. , 2012, Developmental psychobiology.

[7]  Lars Nyberg,et al.  Brain simulation of action may be grounded in physical experience , 2011, Neurocase.

[8]  Valeria Della-Maggiore,et al.  Motor resonance may originate from sensorimotor experience. , 2010, Journal of neurophysiology.

[9]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[10]  S. Wellek.  Testing Statistical Hypotheses of Equivalence and Noninferiority , 2010 .

[11]  M. E. McCarty,et al.  Reaching beyond spatial perception: Effects of intended future actions on visually guided prehension , 2004 .

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

[13]  C. Urgesi,et al.  Action anticipation and motor resonance in elite basketball players , 2008, Nature Neuroscience.

[14]  S. Small,et al.  Action observation has a positive impact on rehabilitation of motor deficits after stroke , 2007, NeuroImage.

[15]  S. Riek,et al.  Reliability of the input–output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation , 2001, Journal of Neuroscience Methods.

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

[17]  D. Rosenbaum,et al.  Time course of movement planning: selection of handgrips for object manipulation. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[18]  L. Craighero,et al.  Human motor cortex excitability during the perception of others’ action , 2005, Current Opinion in Neurobiology.

[19]  Miguel Fernandez-del-Olmo,et al.  Movement observation specifies motor programs activated by the action observed objective , 2011, Neuroscience Letters.

[20]  Umberto Castiello,et al.  Grasping with tools: corticospinal excitability reflects observed hand movements. , 2012, Cerebral cortex.

[21]  Christian Keysers,et al.  Mapping the flow of information within the putative mirror neuron system during gesture observation , 2011, NeuroImage.

[22]  J. P. Morgan,et al.  Design and Analysis: A Researcher's Handbook , 2005, Technometrics.

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

[24]  U. Ziemann,et al.  Cortico-motoneuronal excitation of three hand muscles determined by a novel penta-stimulation technique. , 2004, Brain : a journal of neurology.

[25]  F. Baldissera,et al.  Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement , 2005, Brain Research.

[26]  U. Ziemann,et al.  Estimated magnitude and interactions of cortico-motoneuronal and Ia afferent input to spinal motoneurones of the human hand , 2004, Neuroscience Letters.

[27]  C. Capaday,et al.  Input-output properties and gain changes in the human corticospinal pathway , 1997, Experimental Brain Research.

[28]  R. L. Linscheid,et al.  EMG study of hand muscle recruitment during hard hammer percussion manufacture of Oldowan tools. , 1998, American journal of physical anthropology.

[29]  Zixiang Wang,et al.  I know what you are doing , 2014 .

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

[31]  Umberto Castiello,et al.  Motor cortex excitability is tightly coupled to observed movements , 2012, Neuropsychologia.

[32]  Ricarda I Schubotz,et al.  Neural changes when actions change: Adaptation of strong and weak expectations , 2013, Human brain mapping.

[33]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[34]  G. Sandini,et al.  The mirror-neurons system: data and models. , 2007, Progress in brain research.

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

[36]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[37]  G. Rizzolatti,et al.  Grasping objects and grasping action meanings: the dual role of monkey rostroventral premotor cortex (area F5). , 1998, Novartis Foundation symposium.

[38]  G. Rizzolatti,et al.  Visuomotor neurons: ambiguity of the discharge or 'motor' perception? , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  R. Johansson,et al.  Action plans used in action observation , 2003, Nature.

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

[41]  S. Swinnen,et al.  Observing how others lift light or heavy objects: time-dependent encoding of grip force in the primary motor cortex , 2012, Psychological research.

[42]  Luciano Fadiga,et al.  Effect of weight-related labels on corticospinal excitability during observation of grasping: a TMS study , 2011, Experimental Brain Research.

[43]  S. Wellek,et al.  Elements of Significance Testing with Equivalence Problems , 1991, Methods of Information in Medicine.

[44]  Dennis C. Tkach,et al.  Congruent Activity during Action and Action Observation in Motor Cortex , 2007, The Journal of Neuroscience.

[45]  T. Tsuji,et al.  Functional demanded excitability changes of human hand motor area , 2006, Experimental Brain Research.

[46]  Luciano Fadiga,et al.  New insights on sensorimotor integration: From hand action to speech perception , 2003, Brain and Cognition.

[47]  U. Castiello,et al.  Differential cortical activity for precision and whole‐hand visually guided grasping in humans , 2007, The European journal of neuroscience.

[48]  S. Swinnen,et al.  Observing how others lift light or heavy objects: Which visual cues mediate the encoding of muscular force in the primary motor cortex? , 2010, Neuropsychologia.

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

[50]  F. Pulvermüller,et al.  The time course of action and action-word comprehension in the human brain as revealed by neurophysiology , 2008, Journal of Physiology-Paris.

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

[52]  Marco Davare,et al.  Causal Connectivity between the Human Anterior Intraparietal Area and Premotor Cortex during Grasp , 2010, Current Biology.