Distance and Direction Codes Underlie Navigation of a Novel Semantic Space in the Human Brain

A recent proposal posits that humans might use the same neuronal machinery to support the representation of both spatial and non-spatial information, organizing concepts and memories using spatial codes. This view predicts that the same neuronal coding schemes characterizing navigation in the physical space (tuned to distance and direction) should underlie navigation of abstract semantic spaces, even if they are categorical and labeled by symbols. We constructed an artificial semantic environment by parsing a bidimensional audiovisual object space into four labeled categories. Before and after a nonspatial symbolic categorization training, 25 adults (15 females) were presented with pseudorandom sequences of objects and words during a functional MRI session. We reasoned that subsequent presentations of stimuli (either objects or words) referring to different categories implied implicit movements in the novel semantic space, and that such movements subtended specific distances and directions. Using whole-brain fMRI adaptation and searchlight model-based representational similarity analysis, we found evidence of both distance-based and direction-based responses in brain regions typically involved in spatial navigation: the medial prefrontal cortex and the right entorhinal cortex (EHC). After training, both regions encoded the distances between concepts, making it possible to recover a faithful bidimensional representation of the semantic space directly from their multivariate activity patterns, whereas the right EHC also exhibited a periodic modulation as a function of traveled direction. Our results indicate that the brain regions and coding schemes supporting relations and movements between spatial locations in mammals are recycled in humans to represent a bidimensional multisensory conceptual space during a symbolic categorization task.