State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices.

A transcranial magnetic stimulation (TMS) adaptation paradigm was used to investigate the neural representation of observed motor behavior in the inferior parietal lobule (IPL), ventral premotor cortex (PMv), and in the cortex around the superior temporal sulcus (STS). Participants were shown adapting movies of a hand or a foot acting on different objects and were asked to compare to the movie, a motor act shown in test pictures. The invariant features between adapting and test stimuli fitted a 2 x 2 design: same or different action made by the same or different effector. Neuronavigated TMS pulses were delivered at the onset of each test picture. TMS over the left and right PMv and over the left IPL induced a selective shortening of reaction times (RTs) to stimuli showing a repeated (adapted) action, regardless of the effector performing it. In a second experiment, TMS applied over the left STS induced shortening of RTs for adapted actions but only if also the effector was repeated. The results indicate that observed motor behavior is encoded with the body part that performs it in the temporal lobe. A hierarchically higher level of representation is carried by neural populations in the parietofrontal regions, where acts are encoded in an abstract way.

[1]  M HERSHENSON,et al.  Reaction time as a measure of intersensory facilitation. , 1962, Journal of experimental psychology.

[2]  K. Heilman,et al.  Two forms of ideomotor apraxia , 1982, Neurology.

[3]  K M Heilman,et al.  Pantomime comprehension and ideomotor apraxia. , 1985, Journal of neurology, neurosurgery, and psychiatry.

[4]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[5]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[6]  G E Alexander,et al.  Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. , 1990, Journal of neurophysiology.

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

[8]  C. A. Marzi,et al.  Transcranial magnetic stimulation selectively impairs interhemispheric transfer of visuo-motor information in humans , 1998, Experimental Brain Research.

[9]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

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

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

[12]  P M Rossini,et al.  The role of the left frontal lobe in action naming: rTMS evidence , 2002, Neurology.

[13]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

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

[16]  M. Sereno,et al.  Point-Light Biological Motion Perception Activates Human Premotor Cortex , 2004, The Journal of Neuroscience.

[17]  Elizabeth Bates,et al.  Action comprehension in aphasia: linguistic and non-linguistic deficits and their lesion correlates , 2004, Neuropsychologia.

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

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

[20]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[21]  J. Mazziotta,et al.  Grasping the Intentions of Others with One's Own Mirror Neuron System , 2005, PLoS biology.

[22]  Á. Pascual-Leone,et al.  Repetitive TMS over posterior STS disrupts perception of biological motion , 2005, Vision Research.

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

[24]  Roland Sparing,et al.  Enhancing Picture Naming with Transcranial Magnetic Stimulation , 2006, Behavioural neurology.

[25]  Scott T. Grafton,et al.  Goal Representation in Human Anterior Intraparietal Sulcus , 2006, The Journal of Neuroscience.

[26]  M. Candidi,et al.  Representation of body identity and body actions in extrastriate body area and ventral premotor cortex , 2007, Nature Neuroscience.

[27]  A. Saygin Superior temporal and premotor brain areas necessary for biological motion perception. , 2007, Brain : a journal of neurology.

[28]  Aina Puce,et al.  Common and distinct brain activation to viewing dynamic sequences of face and hand movements , 2007, NeuroImage.

[29]  Nadia Bolognini,et al.  Somatic and Motor Components of Action Simulation , 2007, Current Biology.

[30]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[31]  Juha Silvanto,et al.  Neural adaptation reveals state‐dependent effects of transcranial magnetic stimulation , 2007, The European journal of neuroscience.

[32]  Scott T. Grafton,et al.  Evidence for a distributed hierarchy of action representation in the brain. , 2007, Human movement science.

[33]  N. Kanwisher,et al.  fMRI Adaptation Reveals Mirror Neurons in Human Inferior Parietal Cortex , 2008, Current Biology.

[34]  G Rizzolatti,et al.  When pliers become fingers in the monkey motor system , 2008, Proceedings of the National Academy of Sciences.

[35]  V. Walsh,et al.  State-dependency in brain stimulation studies of perception and cognition , 2008, Trends in Cognitive Sciences.

[36]  Neil G. Muggleton,et al.  Testing the validity of the TMS state-dependency approach: Targeting functionally distinct motion-selective neural populations in visual areas V1/V2 and V5/MT+ , 2008, NeuroImage.

[37]  Bradford Z. Mahon,et al.  A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content , 2008, Journal of Physiology-Paris.

[38]  S. Aglioti,et al.  Neural Underpinnings of Gesture Discrimination in Patients with Limb Apraxia , 2008, The Journal of Neuroscience.

[39]  C. Urgesi,et al.  The Neural Basis of Body Form and Body Action Agnosia , 2008, Neuron.

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

[41]  M. Costantini,et al.  Effector- and target-independent representation of observed actions: evidence from incidental repetition priming , 2008, Experimental Brain Research.

[42]  Hans Herzog,et al.  Activation differences in observation of hand movements for imitation or velocity judgement , 2008, Behavioural Brain Research.

[43]  Juha Silvanto,et al.  Using state‐dependency of transcranial magnetic stimulation (TMS) to investigate letter selectivity in the left posterior parietal cortex: a comparison of TMS‐priming and TMS‐adaptation paradigms , 2008, The European journal of neuroscience.

[44]  Silvio Ionta,et al.  Virtual lesion of ventral premotor cortex impairs visual perception of biomechanically possible but not impossible actions , 2008, Social neuroscience.

[45]  R. Goebel,et al.  The brain's intention to imitate: The neurobiology of intentional versus automatic imitation , 2008, Brain Stimulation.

[46]  Marcel Brass,et al.  How do we infer others' goals from non-stereotypic actions? The outcome of context-sensitive inferential processing in right inferior parietal and posterior temporal cortex , 2008, NeuroImage.

[47]  G. Rizzolatti,et al.  Intention Understanding in Autism , 2009, PloS one.

[48]  Luigi Cattaneo,et al.  Correction: Intention Understanding in Autism , 2009, PLoS ONE.

[49]  Emily S. Cross,et al.  Sensitivity of the action observation network to physical and observational learning. , 2008, Cerebral cortex.

[50]  Joseph T. Devlin,et al.  Supramarginal gyrus involvement in visual word recognition , 2009, Cortex.

[51]  D. Perrett,et al.  Visual Adaptation to Goal-directed Hand Actions , 2009, Journal of Cognitive Neuroscience.

[52]  Luigi Cattaneo,et al.  Representation of Goal and Movements without Overt Motor Behavior in the Human Motor Cortex: A Transcranial Magnetic Stimulation Study , 2009, The Journal of Neuroscience.

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

[54]  R. Cohen Kadosh,et al.  Numerical representation in the parietal lobes: abstract or not abstract? , 2009, The Behavioral and brain sciences.

[55]  Juha Silvanto,et al.  TMS-adaptation reveals abstract letter selectivity in the left posterior parietal cortex. , 2009, Cerebral cortex.

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

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

[58]  Scott T. Grafton Embodied Cognition and the Simulation of Action to Understand Others , 2009, Annals of the New York Academy of Sciences.