The hippocampus and dorso-lateral striatum link distinct types of memories through time and space, respectively

Abstract

Several decades of research have established that different kinds of memories result from the activity of discrete neural networks. Studying how these networks process information in experiments that target specific types of mnemonic representations has provided deep insights into memory architecture and its neural underpinnings. However, in natural settings reality confronts organisms with problems that are not neatly compartmentalized. Thus, a critical problem in memory research that still needs to be addressed is how distinct types of memories are ultimately integrated. Here we demonstrate how two memory networks, the hippocampus and dorso-lateral striatum, may accomplish such a goal. The hippocampus supports memory for facts and events, collectively known as declarative memory and often studied as spatial memory in rodents. The dorso-lateral striatum (putamen in primates) provides the basis for habits which are assessed in stimulus-response types of tasks. Expanding previous findings, the current work revealed that the hippocampus and dorso-lateral striatum use time and space in distinct and largely complementary ways to link spatial and habitual representations. Specifically, the hippocampus supported both types of memories when they were formed in temporal juxtaposition even if the learning took place in different environments. In contrast, the lateral striatum supported both types of memories if they were formed in the same environment even if at temporally distinct points. These results reveal for the first time that by using fundamental aspects of experience in specific ways, the hippocampus and dorso-lateral striatum can transcend their attributed roles in information storage. SIGNIFICANCE STATEMENTThe current paradigm in memory research postulates that different types of memories reflected in separate types of behavioural strategies result from activity in distinct neural circuits. However, recent data have shown that when rats concurrently acquired in the same environment hippocampal-dependent spatial navigation and striatal-dependent approach of a visual cue, each of the two types of memories became dependent on both the hippocampus and dorso-lateral striatum. The current work reveals that the hippocampus and dorso-lateral striatum utilize distinct and complementary principles to integrate different types of memories in time and space: the hippocampus links memories formed in temporal proximity, while the lateral striatum links memories formed in the same space.