A topographical organization for action representation in the human brain

Abstract

How the human brain represents distinct motor features into a unique finalized action still remains undefined. Previous models proposed the distinct features of a motor act to be hierarchically organized in separated, but functionally interconnected, cortical areas. Here, we hypothesized that distinct patterns across a wide expanse of cortex may actually subserve a topographically organized coding of different categories of actions that represents, at a higher cognitive level and independently from the distinct motor features, the action and its final aim as a whole. Using functional magnetic resonance imaging and pattern classification approaches on the neural responses of 14 right-handed individuals passively watching short movies of hand-performed tool-mediated, transitive, and meaningful intransitive actions, we were able to discriminate with a high accuracy and characterize the category-specific response patterns. Actions are distinctively coded in distributed and overlapping neural responses within an action-selective network, comprising frontal, parietal, lateral occipital and ventrotemporal regions. This functional organization, that we named action topography, subserves a higher-level and more abstract representation of finalized actions and has the capacity to provide unique representations for multiple categories of actions.

Keywords: action representation; action topography; fMRI; multivariate analysis; pattern classification.

Figure 1

Methodological workflow. BOLD responses to transitive, intransitive, and tool‐mediated actions from the training set were used in a three‐way classifier. The trained classifier tested a different subset of actions to obtain discrimination accuracy, and isolated the most informative regions. The discrimination ability of this network was subsequently tested on an independent stimuli dataset. Refer to Materials and Methods for further details. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

The action‐selective network. The most informative regions described by the three‐way classifier for tool‐mediated (red), transitive (green) and intransitive (blue) discrimination and projected onto an inflated surface template. Magnified views of left prefrontal, temporo‐occipital and superior parietal regions in boxes A, B, and C, respectively.

Figure 3

Specificity of the distributed representations within the action‐selective network. On the left, the heatmap representing the dissimilarity matrix of the different action stimuli and, on the right, the derived hierarchical clustering. Stimuli were depicted in red font for tool‐mediated, in blue font for intransitive and in green font for transitive actions. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Comparative action category‐specific neural responses of a “standard” univariate analysis. Brain regions showing a significant effect for “action category” were projected onto an inflated surface template, as identified by a univariate repeated measure ANOVA (first row). Post hoc direct comparisons between tool‐mediated, intransitive and transitive action categories have been also reported (second, third, and fourth rows). [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]