Chapter 3 - Cortico-hippocampal systems involved in memory and cognition: the PMAT framework

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Abstract

In this chapter, we review evidence that the cortical pathways to the hippocampus appear to extend from two large-scale cortical systems: a posterior medial (PM) system that includes the parahippocampal cortex and retrosplenial cortex, and an anterior temporal (AT) system that includes the perirhinal cortex. This “PMAT” framework accounts for differences in the anatomical and functional connectivity of the medial temporal lobes, which may underpin differences in cognitive function between the systems. The PM and AT systems make distinct contributions to memory and to other cognitive domains, and convergent findings suggest that they are involved in processing information about contexts and items, respectively. In order to support the full complement of memory-guided behavior, the two systems must interact, and the hippocampal and ventromedial prefrontal cortex may serve as sites of integration between the two systems. We conclude that when considering the “connected hippocampus,” inquiry should extend beyond the medial temporal lobes to include the large-scale cortical systems of which they are a part.

Section snippets

Anatomical and Functional Connectivity of the PM and AT Systems

The foundation of the PMAT framework is an extensive body of literature documenting differences in anatomical connectivity among MTL structures (Aggleton, 2011, Burwell, 2000, Kondo et al., 2005; see Ranganath and Ritchey, 2012 for review). The PHC is extensively interconnected with both the PRC and RSC, but PHC and RSC show highly overlapping patterns of cortical and subcortical connectivity that diverge from the PRC. The PHC and RSC are major targets of the cingulum bundle, a white matter

Relationship Between Connectivity and Function

A core assumption of the PMAT framework is that connectivity and task function are intimately related; that is, the function of its region will be constrained by its connectivity with other structures, sometimes referred to as its “connectional fingerprint” (Passingham et al., 2002). In one recent study, we directly tested whether the PMAT framework could explain the recruitment of different cortical areas during memory encoding (Ritchey et al., 2014). Using a data-driven, graph theoretic

Roles of the PM and AT Systems in Memory and Cognition

The work described above demonstrates clear links between connectivity and function within the PM and AT systems. Here, we will summarize evidence regarding the kinds of tasks that tend to recruit these systems, focusing first on the PHC, RSC, and PRC (those cortical areas most closely affiliated with the hippocampus), and then considering how these differences extend to other components of the PM and AT systems.

The Hippocampus

Perhaps not surprisingly, the PM and AT systems must work together in order to support the full complement of memory-guided behavior. The hippocampus is a clear point of connection between the two systems due to its strong connectivity with both systems. As noted above and in Fig. 2, there are parallel cortico-hippocampal pathways linking the PM and AT systems with the entorhinal cortex, CA1, and subiculum (Witter et al., 2000). The dentate gyrus is a major convergence point within the

Conclusions

Adopting the PMAT framework encourages one to think about the hippocampus not as an endpoint, but as a critical interface between two cortical systems that contribute to cognition in fundamentally different ways. These contributions can be understood as the product of complex interactions between brain areas, constrained by anatomy and optimized to support rapid learning in the service of perception, action, and cognition. Although the PMAT framework can explain an extensive body of evidence,

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