I See Your Effort: Force-Related BOLD Effects in an Extended Action Execution-Observation Network Involving the Cerebellum.

Letizia Casiraghi,Adnan A S Alahmadi,Karl Friston,Anita Monteverdi,Egidio D’Angelo,Claudia A M Gandini Wheeler-Kingshott,Fulvia Palesi,Giovanni Savini,Gloria Castellazzi

doi:10.1093/cercor/bhy322

Abstract

Action observation (AO) is crucial for motor planning, imitation learning, and social interaction, but it is not clear whether and how an action execution–observation network (AEON) processes the effort of others engaged in performing actions. In this functional magnetic resonance imaging (fMRI) study, we used a “squeeze ball” task involving different grip forces to investigate whether AEON activation showed similar patterns when executing the task or observing others performing it. Both in action execution, AE (subjects performed the visuomotor task) and action observation, AO (subjects watched a video of the task being performed by someone else), the fMRI signal was detected in cerebral and cerebellar regions. These responses showed various relationships with force mapping onto specific areas of the sensorimotor and cognitive systems. Conjunction analysis of AE and AO was repeated for the “0th” order and linear and nonlinear responses, and revealed multiple AEON nodes remapping the detection of actions, and also effort, of another person onto the observer’s own cerebrocerebellar system. This result implies that the AEON exploits the cerebellum, which is known to process sensorimotor predictions and simulations, performing an internal assessment of forces and integrating information into high-level schemes, providing a crucial substrate for action imitation.

Highlights

Social behavior is based on understanding the actions of others and predicting appropriate reactions and subsequent interactions
BOLD functional magnetic resonance imaging (fMRI) signals were recorded from 12 healthy subjects during one visuomotor and 2 visual tasks for the purpose of comparing brain activation under action executions (AE) and Action observation (AO) conditions, when different GF levels are applied to an object
Within the AO with visual cue (AOvc) condition, perceived GF (pGF) accuracy was higher after magnetic resonance imaging (MRI) (P = 0.003), while no significant differences were found in the AO condition (P = 0.955)

Summary

Introduction

Social behavior is based on understanding the actions of others and predicting appropriate reactions and subsequent interactions. In this context, perceiving the force applied to objects by others is crucial for understanding their intentions, for predicting the success of self-generated actions, and for dynamic movement control in interactions. There is still debate over the question of whether, when observing someone else performing an action, we mirror the actual movement dynamics or its goals (Calvo-Merino et al 2006; Filimon et al 2007; Thompson et al 2007; Hamilton and Grafton 2008; Caspers et al 2010; Cavallo et al 2015; Koul et al 2018). AE and observation have been studied using several techniques (Munzert et al 2009; Sevdalis and Keller 2011; Vanderwert et al 2013; Naish et al 2014; Valchev et al 2015), the neuronal processes involved in mirroring the motor effort of others have still not been fully explored

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Discussion

Conclusion