Toward a conceptualization of retrohippocampal contributions to learning and memory

A wealth of data supports the notion that the hippocampus binds objects and events together in place and time. In support of this function, a cortical circuit that includes the retrosplenial cortex (RSC) and various structures in the parahippocampal region is thought to provide the hippocampus with essential information regarding the physical and temporal context in which the object/event occurs. However, it remains unclear if and how individual components of this so-called `where' circuit make unique contributions to processing context-related information. Here we focus on the RSC and the postrhinal cortex (POR; homologous with parahippocampal cortex (PHC) in primates), two of the most strongly interconnected components of the where pathway and the foci of an increasing amount of recent research. Much of the behavioral evidence to date suggests that RSC and POR/PHC work closely together as a functional unit. We begin by briefly reviewing studies that have investigated the involvement of RSC and POR/PHC in contextual and spatial learning, both of which involve learning associations and relationships between the individual stimuli that compose an environment (i.e., where information). However, we propose that potential differences have been overlooked because most studies to date have relied on behavioral paradigms and experimental approaches that are not well suited for distinguishing between different aspects of information processing. We then consider the anatomical differences between RSC and POR/PHC and emerging behavioral evidence that gives rise to a working model of how these regions may differentially contribute to hippocampal-dependent learning and memory. We then discuss experimental designs and behavioral methods that may be useful in testing the model. Finally, approaches are described that may be valuable in probing the nature of information processing and neuroplasticity in the myriad of local circuits that are nested within the where pathway. (C) 2014 Elsevier Inc. All rights reserved.