Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network

The processing of kinematic information embedded in observed actions is an essential ability for understanding others' behavior. Previous research showed that the action observation network (AON) may encode some action kinematic features. However, our understanding of how direction and velocity...

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Main Authors: Settimio Ziccarelli, Antonino Errante, Leonardo Fogassi
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:NeuroImage
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Online Access:http://www.sciencedirect.com/science/article/pii/S1053811924004361
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author Settimio Ziccarelli
Antonino Errante
Leonardo Fogassi
author_facet Settimio Ziccarelli
Antonino Errante
Leonardo Fogassi
author_sort Settimio Ziccarelli
collection DOAJ
description The processing of kinematic information embedded in observed actions is an essential ability for understanding others' behavior. Previous research showed that the action observation network (AON) may encode some action kinematic features. However, our understanding of how direction and velocity are encoded within the AON is still limited. In this study, we employed event-related fMRI to investigate the neural substrates specifically activated during observation of hand grasping actions presented as point-light displays, performed with different directions (right, left) and velocities (fast, slow). Twenty-three healthy adult participants took part in the study. To identify brain regions differentially recruited by grasping direction and velocity, univariate and multivariate pattern analysis (MVPA) were performed. The results of univariate analysis demonstrate that direction is encoded in occipito-temporal and posterior visual areas, while velocity recruits lateral occipito-temporal, superior parietal and intraparietal areas. Results of MVPA further show: a) a significant decoding accuracy of both velocity and direction at the network level; b) the possibility to decode within lateral occipito-temporal and parietal areas both direction and velocity; c) a contribution of bilateral premotor areas to velocity decoding models. These results indicate that posterior parietal nodes of the AON are mainly involved in coding grasping direction and that premotor regions are crucial for coding grasping velocity, while lateral occipito-temporal cortices play a key role in encoding both parameters. The current findings could have implications for observational-based rehabilitation treatments of patients with motor disorders and artificial intelligence-based hand action recognition models.
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spelling doaj-art-e63fe53ded7b43c1b06b2e0f53c8bcb12024-11-29T06:23:02ZengElsevierNeuroImage1095-95722024-12-01303120939Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation networkSettimio Ziccarelli0Antonino Errante1Leonardo Fogassi2Department of Medicine and Surgery, University of Parma, Parma 43125, ItalyDepartment of Medicine and Surgery, University of Parma, Parma 43125, Italy; Neuroradiology unit, University Hospital of Parma, Parma 43125, Italy.Department of Medicine and Surgery, University of Parma, Parma 43125, Italy; Corresponding author.The processing of kinematic information embedded in observed actions is an essential ability for understanding others' behavior. Previous research showed that the action observation network (AON) may encode some action kinematic features. However, our understanding of how direction and velocity are encoded within the AON is still limited. In this study, we employed event-related fMRI to investigate the neural substrates specifically activated during observation of hand grasping actions presented as point-light displays, performed with different directions (right, left) and velocities (fast, slow). Twenty-three healthy adult participants took part in the study. To identify brain regions differentially recruited by grasping direction and velocity, univariate and multivariate pattern analysis (MVPA) were performed. The results of univariate analysis demonstrate that direction is encoded in occipito-temporal and posterior visual areas, while velocity recruits lateral occipito-temporal, superior parietal and intraparietal areas. Results of MVPA further show: a) a significant decoding accuracy of both velocity and direction at the network level; b) the possibility to decode within lateral occipito-temporal and parietal areas both direction and velocity; c) a contribution of bilateral premotor areas to velocity decoding models. These results indicate that posterior parietal nodes of the AON are mainly involved in coding grasping direction and that premotor regions are crucial for coding grasping velocity, while lateral occipito-temporal cortices play a key role in encoding both parameters. The current findings could have implications for observational-based rehabilitation treatments of patients with motor disorders and artificial intelligence-based hand action recognition models.http://www.sciencedirect.com/science/article/pii/S1053811924004361Biological motionSpeedTrajectoryMirror neuron systemDecodingfMRI
spellingShingle Settimio Ziccarelli
Antonino Errante
Leonardo Fogassi
Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
NeuroImage
Biological motion
Speed
Trajectory
Mirror neuron system
Decoding
fMRI
title Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
title_full Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
title_fullStr Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
title_full_unstemmed Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
title_short Direction and velocity kinematic features of point-light displays grasping actions are differentially coded within the action observation network
title_sort direction and velocity kinematic features of point light displays grasping actions are differentially coded within the action observation network
topic Biological motion
Speed
Trajectory
Mirror neuron system
Decoding
fMRI
url http://www.sciencedirect.com/science/article/pii/S1053811924004361
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AT antoninoerrante directionandvelocitykinematicfeaturesofpointlightdisplaysgraspingactionsaredifferentiallycodedwithintheactionobservationnetwork
AT leonardofogassi directionandvelocitykinematicfeaturesofpointlightdisplaysgraspingactionsaredifferentiallycodedwithintheactionobservationnetwork