Neural dynamics of grip and goal integration during the processing of others’ actions with objects: An ERP study

Abstract

Recent behavioural evidence suggests that when processing others' actions, motor acts and goalrelated information both contribute to action recognition. Yet the neuronal mechanisms underlying the dynamic integration of the two action dimensions remain unclear. this study aims to elucidate the eRp components underlying the processing and integration of grip and goal-related information. the electrophysiological activity of 28 adults was recorded during the processing of object-directed action photographs (e.g., writing with pencil) containing either grip violations (e.g. upright pencil grasped with atypical-grip), goal violations (e.g., upside-down pencil grasped with typical-grip), both grip and goal violations (e.g., upside-down pencil grasped with atypical-grip), or no violations. participants judged whether actions were overall typical or not according to object typical use. Brain activity was sensitive to the congruency between grip and goal information on the N400, reflecting the semantic integration between the two dimensions. On earlier components, brain activity was affected by grip and goal typicality independently. Critically, goal typicality but not grip typicality affected brain activity on the N300, supporting an earlier role of goal-related representations in action recognition. Findings provide new insights on the neural temporal dynamics of the integration of motor acts and goal-related information during the processing of others' actions.Understanding the actions performed by others is a core ability of human beings 1,2 . Yet, actions are no mere movements but organised and goal-directed movements 3,4 . Thus, understanding others' actions does not only imply the processing of the motor act (e.g., both dynamic and static components of reaching and grasping a bottle) but also the recognition of the actor's goal (e.g., to drink or to move it away). Accordingly, observers mainly perceive others' actions in terms of goals 5-8 and may use different sources of information to this end (e.g., dynamic and static component of the motor act 9 ; functional knowledge about objects 10 ; contextual information 11,12 , among others). Although numerous studies have demonstrated that both information about the motor act and information about the goal of the actor are processed during the decoding of others' actions, the precise role of the two types of information in action recognition remains debated.Important theoretical accounts have highlighted the need to consider the processing of others' actions as a dynamic phenomenon 3,13-15 that cannot be fully uncovered without considering the temporal dynamics of motor acts and action goal decoding. The observation of several successive periods of stability in the brain activity (i.e. "micro-state") when visually processing others' actions 16,17 further supports the idea that the decoding of others' actions is a multistep process. In a recent behavioural experiment, we also demonstrated that the involvement of action goal and static motor act information in action recog...

Photographs of Actions: What Makes Them Special Cues to Social Perception

“…There is a broad consensus in the research literature that the processing of observed live actions in the AON provides observers with knowledge of what others are doing and that this is a key skill of social cognition [ 8 , 23 , 24 , 25 , 38 , 42 , 43 ]. There is, however, controversy about the properties of the knowledge conveyed by neural AON activities: is this knowledge only provided by AON activities, or is it dependent on conceptual and semantic processing [ 15 , 44 , 45 , 46 , 47 , 48 , 49 ]? Is it primarily related to understanding the goal of actions [ 3 , 5 , 15 ], or does it relate equally to several elements of actions, such as grips, movements of body parts, somatosensory processes, objects involved, or context [ 50 , 51 , 52 ]?…”

“…An observer, for example, sees another individual grasping an apple and understands that the individual wants to eat the apple. Regarding the timing of processing, the findings suggest that an observed grip is associated with an action goal, including information about an object involved or the action context, from around 250 ms after movement onset [ 46 , 105 ]. Processing in the extrastriate body area (EBA), middle temporal area (MT), and inferior parietal regions takes place in the time window of 120 to 200 ms after the movement onset [ 19 , 46 , 106 , 107 , 108 ].…”

“…These operations are also associated with neural activities in the AON, but if the AON responses to photos were causally related to these operations, then the responses would occur in a later processing time window after the picture onset. The responses that occur in the time window up to about 300 ms after picture onset are fundamentally related to the processing of the incoming visual information [ 46 , 53 , 66 , 70 , 76 , 105 , 141 ].…”

“…The findings on AON responses to specific properties of actions depicted in photos in the early processing time window suggest that these responses are related to perceptual processes [ 46 , 53 , 66 , 70 , 76 , 105 , 141 ]. The visual information provided by an action photo has properties that are processed by visual cortical areas as incomplete body-related information (EBA) and movement-related information (MT) ( Table 1 ).…”

“…The meanings of objects, the recognition of which requires complex knowledge of abstract concepts or sociocultural practices (as is the case with medical syringes, bank notes, or hand mixers), are processed in the ventral visual stream [ 121 ]. Recognizing the meanings of observed or pictured body movements or somatic sensations often requires the inclusion of information from the environment of an action [ 44 , 46 , 105 , 146 , 147 ]. The action of a woman with the palm of her hand on the cheek of a boy, for example, is made understandable by a bottle of sunscreen on a table next to her.…”