Abstract
Appropriate tool–object pairing is a natural part of our lives. When preparing to stir coffee, we know that a hammer is useful for some tasks but that it is not appropriate in this behavioral context. The neural correlates of this context–tool pairing process remain unclear. In the current work, we used event-related electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) to determine neural correlates for differentiating contextually correct and incorrect tool use. Subjects were shown images depicting correct (e.g., spoon used to stir coffee) or incorrect (e.g., hammer used to stir coffee) tool use. We identified distinct regional and temporal activations for identifying incorrect versus correct tool use. The posterior cingulate, insula, and superior temporal gyrus preferentially differentiated incorrect tool–object usage, while occipital, parietal, and frontal areas were active in identifying correct tool use. Source localized EEG analysis confirmed the fMRI data and showed phases of activation, where incorrect tool-use activation (0–200 ms) preceded occipitotemporal activation for correct tool use (300–400 ms). This work extends our previous findings to better identify the neural substrate for contextual evaluation of tool use, and may contribute to our understanding of neurological disorders resulting in tool-use deficits.
Highlights
Regions of the brain showing activation to tools as a distinct class of objects have been well characterized; viewing tools activates regions surrounding the temporal–parietal–occipital junction, extending along the temporal cortex and into parietal and frontal areas
From 100–200 ms post image presentation (Figure 5; Table 4), these activation differences shifted posteriorly to cuneus, lingual gyrus, insula, superior temporal cortex, and were still exclusive to incorrect over correct tool use
We exploited the spatial resolution of functional magnetic resonance imaging (fMRI) and the temporal resolution of EEG to identify the regional activations associated with conceptual knowledge for understanding tool use in correct and incorrect contexts, and how this activation develops over time
Summary
Regions of the brain showing activation to tools as a distinct class of objects have been well characterized; viewing tools activates regions surrounding the temporal–parietal–occipital junction, extending along the temporal cortex and into parietal and frontal areas (for review, see Lewis, 2006) This suggests the existence of a network, primarily along the ventral visual stream (Milner and Goodale, 2008), for the identification and conceptual understanding of tools. The action-related stream, including the posterior parietal cortex, is active even when no overt motor action is required, such as recognition of graspable versus non-graspable objects (Hattori et al, 2009) and manipulable versus non-manipulable objects (Mecklinger et al, 2002) Part of this action knowledge is related to understanding when and when not to use a particular tool. This suggests knowledge of usability of a tool (e.g., fork) on specific objects (e.g., food) but not on all other objects (e.g., lock, nail, etc.)
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