Dataset Information

Action Categories in Lateral Occipitotemporal Cortex Are Organized Along Sociality and Transitivity.

ABSTRACT: How neural specificity for distinct conceptual knowledge categories arises is central for understanding the organization of semantic memory in the human brain. Although there is a large body of research on the neural processing of distinct object categories, the organization of action categories remains largely unknown. In particular, it is unknown whether different action categories follow a specific topographical organization on the cortical surface analogously to the category-specific organization of object knowledge. Here, we tested whether the neural representation of action knowledge is organized in terms of nonsocial versus social and object-unrelated versus object-related actions (sociality and transitivity, respectively, hereafter). We hypothesized a major distinction of sociality and transitivity along dorsal and ventral lateral occipitotemporal cortex (LOTC), respectively. Using fMRI-based multivoxel pattern analysis, we identified neural representations of action information associated with sociality and transitivity in bilateral LOTC. Representational similarity analysis revealed a dissociation between dorsal and ventral LOTC. We found that action representations in dorsal LOTC are segregated along features of sociality, whereas action representations in ventral LOTC are segregated along features of transitivity. In addition, representations of sociality and transitivity features were found more anteriorly in LOTC than representations of specific subtypes of actions, suggesting a posterior-anterior gradient from concrete to abstract action features. These findings elucidate how the neural representations of perceptually and conceptually diverse actions are organized in distinct subsystems in the LOTC.

Significance statement

The lateral occipitotemporal cortex (LOTC) is critically involved in the recognition of objects and actions, but our knowledge about the underlying organizing principles is limited. Here, we discovered a dorsal-ventral distinction of actions in LOTC: dorsal LOTC represents actions based on sociality (how much an action is directed to another person) in proximity to person knowledge. In contrast, ventral LOTC represents actions based on transitivity (how much an action involves the interaction with inanimate objects) in proximity to tools/artifacts in ventral LOTC, suggesting a mutually dependent organization of actions and objects. In addition, we found a posterior-to-anterior organization of the LOTC for concrete and abstract representations, respectively. Our findings provide important insights about the organization of actions in LOTC.

SUBMITTER: Wurm MF

PROVIDER: S-EPMC6596756 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Publications

Action Categories in Lateral Occipitotemporal Cortex Are Organized Along Sociality and Transitivity.

Wurm Moritz F MF Caramazza Alfonso A Lingnau Angelika A

The Journal of neuroscience : the official journal of the Society for Neuroscience 20170101 3

How neural specificity for distinct conceptual knowledge categories arises is central for understanding the organization of semantic memory in the human brain. Although there is a large body of research on the neural processing of distinct object categories, the organization of action categories remains largely unknown. In particular, it is unknown whether different action categories follow a specific topographical organization on the cortical surface analogously to the category-specific organiz ...[more]

PMID: 28100739

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Project description:Many lines of evidence point to a tight linkage between the perceptual and motoric representations of actions. Numerous demonstrations show how the visual perception of an action engages compatible activity in the observer's motor system. This is seen for both intransitive actions (e.g., in the case of unconscious postural imitation) and transitive actions (e.g., grasping an object). Although the discovery of "mirror neurons" in macaques has inspired explanations of these processes in human action behaviors, the evidence for areas in the human brain that similarly form a crossmodal visual/motor representation of actions remains incomplete. To address this, in the present study, participants performed and observed hand actions while being scanned with functional MRI. We took a data-driven approach by applying whole-brain information mapping using a multivoxel pattern analysis (MVPA) classifier, performed on reconstructed representations of the cortical surface. The aim was to identify regions in which local voxelwise patterns of activity can distinguish among different actions, across the visual and motor domains. Experiment 1 tested intransitive, meaningless hand movements, whereas experiment 2 tested object-directed actions (all right-handed). Our analyses of both experiments revealed crossmodal action regions in the lateral occipitotemporal cortex (bilaterally) and in the left postcentral gyrus/anterior parietal cortex. Furthermore, in experiment 2 we identified a gradient of bias in the patterns of information in the left hemisphere postcentral/parietal region. The postcentral gyrus carried more information about the effectors used to carry out the action (fingers vs. whole hand), whereas anterior parietal regions carried more information about the goal of the action (lift vs. punch). Taken together, these results provide evidence for common neural coding in these areas of the visual and motor aspects of actions, and demonstrate further how MVPA can contribute to our understanding of the nature of distributed neural representations.

Project description:Human visual cortex is organized with striking consistency across individuals. While recent findings demonstrate an unexpected coupling between functional and cytoarchitectonic regions relative to the folding of human visual cortex, a unifying principle linking these anatomical and functional features of the cortex remains elusive. To fill this gap in knowledge, we combined independent and ground truth measurements of cytoarchitectonic regions and genetic tissue characterization within human occipitotemporal cortex. Using a data-driven approach, we examined whether differential gene expression among cytoarchitectonic areas could contribute to the arealization of occipitotemporal cortex into a hierarchy based on transcriptomics. This approach revealed two opposing gene expression gradients: one that contains a series of genes with expression magnitudes that ascend from posterior (e.g., areas human occipital [hOc]1, hOc2, hOc3, etc.) to anterior cytoarchitectonic areas (e.g., areas fusiform gyrus [FG]1-FG4) and another that contains a separate series of genes that show a descending gradient from posterior to anterior areas. Using data from the living human brain, we show that each of these gradients correlates strongly with variations in measures related to either thickness or myelination of cortex, respectively. We further reveal that these genetic gradients emerge along unique trajectories in human development: the ascending gradient is present at 10-12 gestational weeks, while the descending gradient emerges later (19-24 gestational weeks). Interestingly, it is not until early childhood (before 5 years of age) that the two expression gradients achieve their adult-like mean expression values. Additional analyses in nonhuman primates (NHPs) reveal that homologous genes do not generate the same ascending and descending expression gradients as in humans. We discuss these findings relative to previously proposed hierarchies based on functional and cytoarchitectonic features of visual cortex. Altogether, these findings bridge macroscopic features of human cytoarchitectonic areas in visual cortex with microscopic features of cellular organization and genetic expression, which, despite the complexity of this multiscale correspondence, can be described by a sparse subset (approximately 200) of genes. These findings help pinpoint the genes contributing to healthy cortical development and explicate the cortical biology distinguishing humans from other primates, as well as establishing essential groundwork for understanding future work linking genetic mutations with the function and development of the human brain.

Dataset Information

Action Categories in Lateral Occipitotemporal Cortex Are Organized Along Sociality and Transitivity.

Significance statement

Publications

Action Categories in Lateral Occipitotemporal Cortex Are Organized Along Sociality and Transitivity.

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