The Representation of Observed Actions at the Subordinate, Basic, and Superordinate Level

J Neurosci. 2023 Nov 29;43(48):8219-8230. doi: 10.1523/JNEUROSCI.0700-22.2023.

Abstract

Actions can be planned and recognized at different hierarchical levels, ranging from very specific (e.g., to swim backstroke) to very broad (e.g., locomotion). Understanding the corresponding neural representation is an important prerequisite to reveal how our brain flexibly assigns meaning to the world around us. To address this question, we conducted an event-related fMRI study in male and female human participants in which we examined distinct representations of observed actions at the subordinate, basic and superordinate level. Using multiple regression representational similarity analysis (RSA) in predefined regions of interest, we found that the three different taxonomic levels were best captured by patterns of activations in bilateral lateral occipitotemporal cortex (LOTC), showing the highest similarity with the basic level model. A whole-brain multiple regression RSA revealed that information unique to the basic level was captured by patterns of activation in dorsal and ventral portions of the LOTC and in parietal regions. By contrast, the unique information for the subordinate level was limited to bilateral occipitotemporal cortex, while no single cluster was obtained that captured unique information for the superordinate level. The behaviorally established action space was best captured by patterns of activation in the LOTC and superior parietal cortex, and the corresponding neural patterns of activation showed the highest similarity with patterns of activation corresponding to the basic level model. Together, our results suggest that occipitotemporal cortex shows a preference for the basic level model, with flexible access across the subordinate and the basic level.SIGNIFICANCE STATEMENT The human brain captures information at varying levels of abstraction. It is debated which brain regions host representations across different hierarchical levels, with some studies emphasizing parietal and premotor regions, while other studies highlight the role of the lateral occipitotemporal cortex (LOTC). To shed light on this debate, here we examined the representation of observed actions at the three taxonomic levels suggested by Rosch et al. (1976) Our results highlight the role of the LOTC, which hosts a shared representation across the subordinate and the basic level, with the highest similarity with the basic level model. These results shed new light on the hierarchical organization of observed actions and provide insights into the neural basis underlying the basic level advantage.

Keywords: action categorization; action observation; action recognition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain Mapping
  • Cerebral Cortex / physiology
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Occipital Lobe* / physiology
  • Parietal Lobe
  • Pattern Recognition, Visual / physiology
  • Temporal Lobe* / physiology