Toward a conceptualization of retrohippocampal contributions to learning and memory

Abstract

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.

Retrosplenial cortex is required for the retrieval of remote memory for auditory cues

“…To date, most studies have focused on the involvement of RSC in spatial and contextual memory (for reviews, see Vann et al 2009;Bucci and Robinson 2014;Miller et al 2014;, given the known connectivity between RSC and visuo-spatial cortical regions (van Groen and Wyss 1990, 1992, 2003. Here we extend this work by demonstrating for the first time that manipulations of RSC impair remote memory for discrete auditory cues.…”

The retrosplenial cortex is involved in the formation of memory for context and trace fear conditioning

“…Although it unclear why trace fear conditioning recruits the RSC in addition to the prefrontal cortex and hippocampus, it is possible that the complex temporal relationship between the CS and UCS in trace conditioning is processed by the RSC. Indeed, the RSC is thought to be a key structure in the where/when pathway, delivering information about the physical and temporal context to the hippocampus (Bucci & Robinson, 2014; Todd & Bucci, In Press). It is therefore tempting to speculate that when the demands of the learning task require significant where/when processing, as occurs in trace or context fear conditioning, the RSC is recruited for acquisition.…”

Higher-order conditioning and the retrosplenial cortex

“…The fact that the RSC receives input from both visual and auditory sensory cortices suggests that it is well-placed to contribute to learning and memory in situations that require processing multiple stimuli from different modalities. Indeed, it has been suggested that the RSC is specifically involved in forming associations between multiple stimuli, or stimulus-stimulus (S-S) learning (e.g., Bucci & Robinson, 2014). Consistent with this idea, two previous studies from our lab have demonstrated a role for the RSC in a different form of higher-order conditioning, sensory preconditioning (e.g., Robinson et al, 2012, 2014).…”

“…A growing body of research has demonstrated that the retrosplenial cortex (RSC) makes important contributions to spatial and contextual learning and memory (for reviews see Bucci & Robinson, 2014; Miller, Vedder, Law, & Smith, 2014; Todd & Bucci, 2015; Vann, Aggleton, & Maguire, 2009). For example, the RSC is necessary for acquisition and retrieval of contextual fear conditioning (Corcoran et al, 2011; Keene & Bucci, 2008a, 2008c; Kwapis et al, 2015), as well as encoding and retrieval of spatial information (Czajkowski et al, 2014).…”

“…First, the RSC receives input from multiple sensory association areas, making it likely to contribute to learning and memory in situations that involve multiple cues (e.g., Keene & Bucci, 2008b), such as second-order conditioning. Second, one recent conceptualization of RSC function is that it is specifically involved in conjointly processing and associating sensory stimuli, even in the absence of primary reinforcement (e.g., Bucci & Robinson, 2014). Thus, both of these related approaches suggest the RSC should contribute to second-order fear conditioning.…”