Ventral encoding of functional affordances: A neural pathway for identifying errors in action

•fMRI was used to determine brain activation in understanding tool manipulation.•Ventral but not dorsal areas were important for understanding incorrect tool use.•Ventral stream areas may code the functional relevance of action affordances. Functional tool usage is a critical aspect of our daily lives. Not only must we know which tools to use for a specific action goal, we must also know how to manipulate those tools in meaningful way to achieve the goal of the action. The purpose of this study was to identify the regions of the brain critical to supporting the process of understanding errors in tool manipulation. Using fMRI, neural activations were recorded while subjects were presented with images demonstrating typical action scenes (screwdriver used on a screw), but with the tool being manipulated either correctly (screwdriver held by handle) or incorrectly (screwdriver held by bit rather than handle). Activations in fMRI for identifying correct over incorrect tool manipulation were seen along the canonical parietofrontal action network, while activations for identifying incorrect over correct tool manipulation were primarily seen at superior temporal areas and insula. We expand our hypotheses about ventral brain networks identifying contextual error to further suggest mechanisms for understanding functional tool actions, which collectively we regard as functional affordances. This proposes a fundamental role for ventral brain areas in functional action understanding.