Dataset Information

Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension.

ABSTRACT: Understanding object-directed actions performed by others is central to everyday life. This ability is thought to rely on the interaction between the dorsal action observation network (AON) and a ventral object recognition pathway. On this view, the AON would encode action kinematics, and the ventral pathway, the most likely intention afforded by the objects. However, experimental evidence supporting this model is still scarce. Here, we aimed to disentangle the contribution of dorsal vs. ventral pathways to action comprehension by exploiting their differential tuning to low-spatial frequencies (LSFs) and high-spatial frequencies (HSFs). We filtered naturalistic action images to contain only LSF or HSF and measured behavioral performance and corticospinal excitability (CSE) using transcranial magnetic stimulation (TMS). Actions were embedded in congruent or incongruent scenarios as defined by the compatibility between grips and intentions afforded by the contextual objects. Behaviorally, participants were better at discriminating congruent actions in intact than LSF images. This effect was reversed for incongruent actions, with better performance for LSF than intact and HSF. These modulations were mirrored at the neurophysiological level, with greater CSE facilitation for congruent than incongruent actions for HSF and the opposite pattern for LSF images. Finally, only for LSF did we observe CSE modulations according to grip kinematics. While results point to differential dorsal (LSF) and ventral (HSF) contributions to action comprehension for grip and context encoding, respectively, the negative congruency effect for LSF images suggests that object processing may influence action perception not only through ventral-to-dorsal connections, but also through a dorsal-to-dorsal route involved in predictive processing.

SUBMITTER: Amoruso L

PROVIDER: S-EPMC7293594 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension.

Amoruso Lucia L Finisguerra Alessandra A Urgesi Cosimo C

Proceedings of the National Academy of Sciences of the United States of America 20200526 23

Understanding object-directed actions performed by others is central to everyday life. This ability is thought to rely on the interaction between the dorsal action observation network (AON) and a ventral object recognition pathway. On this view, the AON would encode action kinematics, and the ventral pathway, the most likely intention afforded by the objects. However, experimental evidence supporting this model is still scarce. Here, we aimed to disentangle the contribution of dorsal vs. ventral ...[more]

PMID: 32457158

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Project description:Visual perception of actions and objects has been shown to activate different cortical systems: action perception system spanning more dorsally, across parietal, frontal, and dorsal temporal regions; object perception relying more strongly the ventral occipitotemporal cortex (VOTC). Compared to the well-established object-domain structure (e.g., faces vs. artifacts) in VOTC, it is less known whether the action perception system is constrained by similar domain principle and whether it communicates with the ventral object recognition system in a domain-specific manner. In a fMRI long-block experiment designed to evaluate both regional activity and task-based functional connectivity (FC) patterns, participants viewed animated videos of a human performing two domains of actions to the same set of meaningless shapes without object-domain information: social-communicative-actions (e.g., waving) and manipulation-actions (e.g., folding). We observed action-domain-specific activations, with the superior temporal sulcus and the right precentral region responding more strongly during social-communicative-action perception; the supramarginal gyrus, inferior and superior parietal lobe, and precentral gyrus during manipulation-action perception. The two domains of action perception systems communicated with VOTC in domain-specific manners: FC between the social-communicative-action system and the bilateral fusiform face area was enhanced during social-communicative-action perception; FC between the manipulation-action system and the left tool-preferring lateral occipitoptemporal cortex was enhanced during manipulation-action perception. There was a significant correlation between the FC-with-action-system and the local activity strength across VOTC voxels. Our findings highlight social- and manipulation-domains of human interaction as an overarching principle of both object and action perception systems, with domain-based functional communication across systems.

Dataset Information

Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension.

Publications

Spatial frequency tuning of motor responses reveals differential contribution of dorsal and ventral systems to action comprehension.

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