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

J Neurosci. 2017 Jan 18;37(3):562-575. doi: 10.1523/JNEUROSCI.1717-16.2016.

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.

Keywords: MVPA; action observation; categories; fMRI; occipitotemporal cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping / methods*
  • Female
  • Humans
  • Male
  • Occipital Lobe / physiology*
  • Pattern Recognition, Visual / physiology*
  • Photic Stimulation / methods
  • Psychomotor Performance / physiology*
  • Social Behavior*
  • Temporal Lobe / physiology*
  • Young Adult