Movement kinematics drive chain selection toward intention detection

Significance Estimation of intentions from the observation of other people’s actions has been proposed to rely on the same motor chain organization supporting the execution of intentional actions. However, the nature of the mechanism by which a specific neuronal chain is selected among possible alternatives during action observation remains obscure. Our study shows that in absence of discriminative contextual cues, subtle changes in the kinematics of the observed action inform mapping to the most probable chain. These results shed light on the importance of kinematics for the attribution of intentions to actions. The ability to understand intentions based on another’s movements is crucial for human interaction. This ability has been ascribed to the so-called motor chaining mechanism: anytime a motor chain is activated (e.g., grasp-to-drink), the observer attributes to the agent the corresponding intention (i.e., to drink) from the first motor act (i.e., the grasp). However, the mechanisms by which a specific chain is selected in the observer remain poorly understood. In the current study, we investigate the possibility that in the absence of discriminative contextual cues, slight kinematic variations in the observed grasp inform mapping to the most probable chain. Chaining of motor acts predicts that, in a sequential grasping task (e.g., grasp-to-drink), electromyographic (EMG) components that are required for the final act [e.g., the mouth-opening mylohyoid (MH) muscle] show anticipatory activation. To test this prediction, we used MH EMG, transcranial magnetic stimulation (TMS; MH motor-evoked potentials), and predictive models of movement kinematics to measure the level and timing of MH activation during the execution (Experiment 1) and the observation (Experiment 2) of reach-to-grasp actions. We found that MH-related corticobulbar excitability during grasping observation varied as a function of the goal (to drink or to pour) and the kinematics of the observed grasp. These results show that subtle changes in movement kinematics drive the selection of the most probable motor chain, allowing the observer to link an observed act to the agent’s intention.

[1]  C. Becchio,et al.  The visible face of intention: why kinematics matters , 2014, Front. Psychol..

[2]  Pierre Jacob,et al.  How from action-mirroring to intention-ascription? , 2013, Consciousness and Cognition.

[3]  P Moirot,et al.  Mylohyoid motor‐evoked potentials relate to swallowing function after chronic stroke dysphagia , 2007, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[4]  James M. Kilner,et al.  Learning to understand others' actions , 2010, Biology Letters.

[5]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[6]  J. Decety,et al.  From the perception of action to the understanding of intention , 2001, Nature reviews. Neuroscience.

[7]  David B. MacDonald,et al.  Intraoperative Motor Evoked Potential Monitoring: Overview and Update , 2006, Journal of Clinical Monitoring and Computing.

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

[9]  M Hallett,et al.  Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. , 1997, Electroencephalography and clinical neurophysiology.

[10]  Massimiliano Pontil,et al.  Action Observation Areas Represent Intentions From Subtle Kinematic Features , 2018, Cerebral cortex.

[11]  C. Heyes,et al.  Mirror neurons: from origin to function. , 2014, The Behavioral and brain sciences.

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

[13]  A. Hamilton,et al.  Reflecting on the mirror neuron system in autism: A systematic review of current theories , 2013, Developmental Cognitive Neuroscience.

[14]  Scott T. Grafton.  The cognitive neuroscience of prehension: recent developments , 2010, Experimental Brain Research.

[15]  Cristina Becchio,et al.  Seeing mental states: An experimental strategy for measuring the observability of other minds. , 2017, Physics of life reviews.

[16]  Sverker Runeson,et al.  Perceiving people through their movements , 1985 .

[17]  R. Lemon,et al.  What We Know Currently about Mirror Neurons , 2013, Current Biology.

[18]  Salvatore Maria Aglioti,et al.  The bright and the dark sides of motor simulation , 2017, Neuropsychologia.

[19]  Antonino Casile,et al.  Human movements and abstract motion displays activate different processes in the observer's motor system , 2016, NeuroImage.

[20]  S. Blakemore,et al.  Dynamic Modulation of Human Motor Activity When Observing Actions , 2011, The Journal of Neuroscience.

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

[22]  James M. Kilner,et al.  More than one pathway to action understanding , 2011, Trends in Cognitive Sciences.

[23]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[24]  Leonardo Fogassi,et al.  Neuronal Chains for Actions in the Parietal Lobe: A Computational Model , 2011, PloS one.

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

[26]  Won Hyuk Chang,et al.  Effects of Bilateral Repetitive Transcranial Magnetic Stimulation on Post-Stroke Dysphagia , 2017, Brain Stimulation.

[27]  G. Rizzolatti,et al.  Impairment of actions chains in autism and its possible role in intention understanding , 2007, Proceedings of the National Academy of Sciences.

[28]  Cristina Becchio,et al.  The observability principle and beyond: Reply to comments on "Seeing mental states: An experimental strategy for measuring the observability of other minds" by Cristina Becchio et al. , 2018, Physics of life reviews.

[29]  N. Holmes,et al.  To eat or not to eat? Kinematics and muscle activity of reach-to-grasp movements are influenced by the action goal, but observers do not detect these differences , 2013, Experimental Brain Research.

[30]  Cristina Becchio,et al.  Decoding intentions from movement kinematics , 2016, Scientific Reports.

[31]  Yuan Yang,et al.  Predicting Object Size from Hand Kinematics: A Temporal Perspective , 2015, PloS one.

[32]  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.

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

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

[35]  G. Rizzolatti,et al.  The Dynamics of Sensorimotor Cortical Oscillations during the Observation of Hand Movements: An EEG Study , 2012, PloS one.