Sequential involvements of the perirhinal cortex and hippocampus in the recall of item-location associative memory in macaques

Abstract

The standard consolidation theory suggests that the hippocampus (HPC) is critically involved in acquiring new memory, while storage and recall gradually become independent of it. Converging studies have shown separate involvements of the perirhinal cortex (PRC) and parahippocampal cortex (PHC) in item and spatial processes, whereas HPC relates the item to a spatial context. These 2 strands of literature raise the following question; which brain region is involved in the recall process of item-location associative memory? To solve this question, this study applied an item-location associative (ILA) paradigm in a single-unit study of nonhuman primates. We trained 2 macaques to associate 4 visual item pairs with 4 locations on a background map in an allocentric manner before the recording sessions. In each trial, 1 visual item and the map image at a tilt (−90° to 90°) 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 the PRC, PHC, 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, followed by the HPC and PHC. We examined whether neural representations of the retrieved locations were related to the external space that the macaques viewed. A positive representation similarity was found in the HPC and PHC, but not in the PRC, thus suggesting a contribution of the HPC to relate the retrieved location from the PRC with a first-person perspective of the subjects and provide the self-referenced retrieved location to the PHC. These results imply distinct but complementary contributions of the PRC and HPC to recall of item-location associative memory that can be used across multiple spatial contexts.