Context and hand posture modulate the neural dynamics of tool–object perception

Prior research has linked visual perception of tools with plausible motor strategies. Thus, observing a tool activates the putative action-stream, including the left posterior parietal cortex. Observing a hand functionally grasping a tool involves the inferior frontal cortex. However, tool-use movements are performed in a contextual and grasp specific manner, rather than relative isolation. Our prior behavioral data has demonstrated that the context of tool-use (by pairing the tool with different objects) and varying hand grasp postures of the tool can interact to modulate subjects' reaction times while evaluating tool-object content. Specifically, perceptual judgment was delayed in the evaluation of functional tool-object pairings (Correct context) when the tool was non-functionally (Manipulative) grasped. Here, we hypothesized that this behavioral interference seen with the Manipulative posture would be due to increased and extended left parietofrontal activity possibly underlying motor simulations when resolving action conflict due to this particular grasp at time scales relevant to the behavioral data. Further, we hypothesized that this neural effect will be restricted to the Correct tool-object context wherein action affordances are at a maximum. 64-channel electroencephalography (EEG) was recorded from 16 right-handed subjects while viewing images depicting three classes of tool-object contexts: functionally Correct (e.g. coffee pot-coffee mug), functionally Incorrect (e.g. coffee pot-marker) and Spatial (coffee pot-milk). The Spatial context pairs a tool and object that would not functionally match, but may commonly appear in the same scene. These three contexts were modified by hand interaction: No Hand, Static Hand near the tool, Functional Hand posture and Manipulative Hand posture. The Manipulative posture is convenient for relocating a tool but does not afford a functional engagement of the tool on the target object. Subjects were instructed to visually assess whether the pictures displayed correct tool-object associations. EEG data was analyzed in time-voltage and time-frequency domains. Overall, Static Hand, Functional and Manipulative postures cause early activation (100-400ms post image onset) of parietofrontal areas, to varying intensity in each context, when compared to the No Hand control condition. However, when context is Correct, only the Manipulative Posture significantly induces extended neural responses, predominantly over right parietal and right frontal areas [400-600ms post image onset]. Significant power increase was observed in the theta band [4-8Hz] over the right frontal area, [0-500ms]. In addition, when context is Spatial, Manipulative posture alone significantly induces extended neural responses, over bilateral parietofrontal and left motor areas [400-600ms]. Significant power decrease occurred primarily in beta bands [12-16, 20-25Hz] over the aforementioned brain areas [400-600ms]. Here, we demonstrate that the neural processing of tool-object perception is sensitive to several factors. While both Functional and Manipulative postures in Correct context engage predominantly an early left parietofrontal circuit, the Manipulative posture alone extends the neural response and transitions to a late right parietofrontal network. This suggests engagement of a right neural system to evaluate action affordances when hand posture does not support action (Manipulative). Additionally, when tool-use context is ambiguous (Spatial context), there is increased bilateral parietofrontal activation and, extended neural response for the Manipulative posture. These results point to the existence of other networks evaluating tool-object associations when motoric affordances are not readily apparent and underlie corresponding delayed perceptual judgment in our prior behavioral data wherein Manipulative postures had exclusively interfered in judging tool-object content.