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.

Autistic Traits Differently Account for Context-Based Predictions of Physical and Social Events

“…Indeed, observing actions embedded in contexts that are congruent or incongruent with the unfolding kinematics, respectively, facilitated or inhibited discrimination performance and motor activation, as compared to observing actions embedded in an ambiguous context [14][15][16]. Notably, lower sensitivity to contextual information and higher reliance on the sensory evidence provided by kinematics were found in individuals with higher autistic traits [16], in particular in the domains of Social skills and Attention to details [16,36]. This points to an association between both social and non-social aspects of autistic traits and impairments in the integration of sensory evidence and contextual information.…”

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 ]?…”

“…Rizzolatti and Craighero [ 104 ] spoke of the “semantics” (p. 184) of the mirror neuron system. Action categorization is assumed to involve interactions between the AON and areas of the ventral visual stream [ 43 , 44 , 45 , 48 , 49 , 50 ]. These interactions run via neural bi-directional connections that give the AON access to conceptual and semantic information.…”

“…Categorization involves generalization and a massive reduction of the information that is received and processed. Neural responses in the AON presumably also reflect the formation of motor and/or somatosensory activation patterns that represent specific properties of the observed actions more comprehensively than categories [ 8 , 36 , 44 , 50 , 54 ]. Specific properties of actions, for example, relate to properties of grips, movements, somatosensory activities, body postures, or objects.…”

“…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.…”