Distributed and integrated representations of tools in human parietal and anterior temporal regions revealed by fMRI-RSA

Abstract

Classical models of tool knowledge and use are centred on dorsal and ventral parietal pathways. Theories of semantic cognition implicate a "hub-and-spoke" network, centred on the anterior temporal lobe (ATL), that underpins all concepts including tools. Despite their prominence, the two theoretical frameworks have never been brought together and the large discrepancy in the functional neuroanatomy addressed. We undertook a multiple-regression Representational Similarity Analysis (RSA) of task fMRI data with four (motor action, broad function, mechanical function, object structure) feature-based models. The motor action model correlated with the activation patterns in bilateral superior parietal lobules (SPL), while the models of broad function and mechanical effect aligned with the activation patterns in bilateral ATLs. The object-structure model correlated with activation patterns in bilateral middle occipital gyri. The results also showed that the ventral ATL activation patterns corresponded simultaneously with all RDM models except object structure. Furthermore, a standard univariate analysis using tool-familiarity ratings for parametric modulation revealed that classical tool-network regions (frontal, inferior parietal, and posterior middle temporal cortices) were increasingly active as the tool familiarity reduced. These results demonstrate that parietal and ATL regions are both crucial and motivate a major extension and revision of the neuroanatomical framework for tool use. Significance StatementThis study provides definitive evidence for convergent tool representation in human anterior temporal lobe (ATL), outside the traditionally focused parietal lobe as the critical centre for human tool-use ability. For many years the parietal lobe was considered crucial in recognizing and planning use of familiar objects, while regions in temporal lobe received little attention. Our advanced multi-voxel analysis with artefact-resistive fMRI scanning revealed that both non-motor (tool-function) and motor (kinematics for tool use) information convergently represented in the left ventral ATL, while showing other distributed regions encoding distinct types of tool information in anterior temporal and parietal regions. These findings highlight the ATLs crucial role in tool representation and necessitate a significant expansion of neuroanatomical framework for human tool-use ability.