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 nonspatial 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.SIGNIFICANCE STATEMENT The hippocampal formation and the medial prefrontal cortex of mammals represent the surrounding physical space by encoding distances and directions between locations. Recent works suggested that humans use the same neural machinery to organize their memories as points of an internal map of experiences. We asked whether the same brain regions and neural codes supporting spatial navigation are recruited when humans use language to organize their knowledge of the world in categorical semantic representations. Using fMRI, we show that the medial prefrontal cortex and the entorhinal portion of the hippocampal formation represent the distances and the movement directions between concepts of a novel audiovisual semantic space, and that it was possible to reconstruct, from neural data, their relationships in memory.