Sequential involvements of macaque perirhinal cortex and hippocampus in semantic-like memory including spatial component

Abstract

The standard consolidation theory suggests the critical involvement of the hippocampus (HPC) in acquiring new knowledge, while the perirhinal cortex (PRC) is involved in its long-term storage (i.e., semantic memory). Converging studies have shown exclusive involvement of the PRC in item processing, while the HPC relates the item with a spatial context. These two lines of literature raise the following question; which brain region is involved in semantic recall that includes the spatial components? To solve this question, we applied an item-location associative (ILA) paradigm in a single-unit study using non-human primates. We trained two macaques to associate four visual item pairs with four locations on a background map before the recording sessions. In each trial, one visual item and the map image at a tilt (-90 to 90 degrees) were sequentially presented as the item-cue and the context-cue, respectively. The macaques chose the item-cue location relative to the context-cue by positioning their gaze. Neurons in both PRC and HPC but not area TE exhibited item-cue responses which signaled retrieval of item-location associative memory. This retrieval signal first appeared in the PRC before appearing in the HPC. We examined whether neural representations of the retrieved locations were related to the external space where the macaques viewed. A positive representation similarity was found in the HPC but not PRC, suggesting a contribution of the HPC to relate the retrieved location with a first-person perspective of the subjects. These results suggest their distinct but complementary contributions to semantic recall including spatial components.