The Role of Attention and Saccades on Parietofrontal Encoding of Contextual and Grasp-specific Affordances of Tools: An ERP Study

Abstract The ability to recognize a tool’s affordances (how a spoon should be appropriately grasped and used), is vital for daily life. Prior research has identified parietofrontal circuits, including mirror neurons, to be critical in understanding affordances. However, parietofrontal action-encoding regions receive extensive visual input and are adjacent to parietofrontal attention control networks. It is unclear how eye movements and attention modulate parietofrontal encoding of affordances. To address this issue, scenes depicting tools in different use-contexts and grasp-postures were presented to healthy subjects across two experiments, with stimuli durations of 100 ms or 500 ms. The 100-ms experiment automatically restricted saccades and required covert attention, while the 500-ms experiment allowed overt attention. The two experiments elicited similar behavioral decisions on tool-use correctness and isolated the influence of attention on parietofrontal activity. Parietofrontal ERPs (P600) distinguishing tool-use contexts (e.g., spoon–yogurt vs. spoon–ball) were similar in both experiments. Conversely, parietofrontal ERPs distinguishing tool-grasps were characterized by posterior to frontal N130-N200 ERPs in the 100-ms experiment and by saccade-perturbed N130-N200 ERPs, frontal N400 and parietal P500 in the 500-ms experiment. Particularly, only overt gaze toward the hand–tool interaction engaged mirror neurons (frontal N400) when discerning grasps that manipulate but not functionally use a tool – (grasp bowl rather than stem of spoon). Results here detail the first human electrophysiological evidence on how attention selectively modulates multiple parietofrontal grasp-perception circuits, especially the mirror neuron system, while unaffecting parietofrontal encoding of tool-use contexts. These results are pertinent to neurophysiological models of affordances that typically neglect the role of attention in action perception.