Context representations, context functions, and the parahippocampal-hippocampal system

Abstract

Psychologists and neurobiologists have a long-standing interest in understanding how the context surrounding the events of our lives is represented and how it influences our behavior. The hippocampal formation emerged very early as a major contributor to how context is represented and functions. There is a large literature examining its contribution that on the surface reveals an array of conflicting outcomes and controversy. This review reveals that these conflicts can be resolved by building Nadel and Willner's dual-process theory of context representations. Two general conclusions emerge: (1) There are two neural systems that can support context representations and functions-a neocortical system composed primarily of perirhinal and postrhinal cortices and a hippocampal system that includes perirhinal, postrhinal, entorhinal cortices, and the hippocampal formation. (2) These two systems are not equivalent-some context representations and functions are uniquely supported by the hippocampal system. These conclusions are discussed in the context of canonical ideas about the special properties of the hippocampal system that enable it to make unique contributions to memory.

Figure 1.

This cartoon illustrates the context pre-exposure facilitation effect discovered by Fanselow (1990). When rats are immediately shocked, they display very little fear of the context. However, if they are pre-exposed to the context, they display fear of that context. (Figure is from Rudy [2008], and reprinted with permission from Sinauer Associates ©2008.)

Figure 2.

Illustration of the object-in-context procedure. (A) In the exploration phase, rats are allowed to explore and sample two objects, a cube and a cylinder. Two cubes were present in one context, and two cylinders were present in the other context. (B) During the test phase, the cube and the cylinder are in each context. Normal rats spent more time exploring the object that had not previously been presented in the test context, indicating a memory for where the object had been previously experienced. (Figure is from Rudy [2008], and reprinted with permission from Sinauer Associates ©2008.)

Figure 3.

Illustration of the dual systems theory of context representations. The elemental association account assumes that the context is represented as a set of individual features (A–D) that independently associate with some event (E). The neocortex is assumed to support elemental context representations. The hierarchical view assumes that the individual elements or features of a context are bound into a representation that functions as a unit to define a place where an event occurs. Hierarchical representations require the hippocampal formation for support.

Figure 4.

A highly schematic illustration of the components of the parahippocampal–hippocampal system (HS) and connections among them. Information is increasingly integrated as it flows from the neocortical associative areas to the parahippocampal regions and the hippocampal formation. The organization of this system also features reciprocal connections with multiple return loops so that information processed in a downstream receiving region is projected back to the sending regions. The hippocampal formation sits at the top of this hierarchical arrangement. (DG) Dentate gyrus; (SUB) subiculum; (EC) entorhinal cortex; (PER) perirhinal cortex; (POR) postrhinal cortex; (PHR) parahippocampal region; (HF) hippocampal formation.

Figure 5.

A highly schematic illustration of the neocortical and hippocampal systems (HS) that support context representations and their connections to the amygdala, which supports freezing. Note that PER and POR cortices can still support contextual fear even if the entorhinal cortex and hippocampal formation are damaged prior to conditioning. However, damage to PER and POR cortices prior to or after contextual fear conditioning deprive the animal of representations needed to support contextual fear. When the hippocampal system is intact, it tends to dominate the neocortical system in the competition for contextual control over fear, as indicated by the strength of the arrows connecting these regions to the amygdala. (NCS) Neocortical system; (HF) hippocampal formation; (EC) entorhinal cortex; (POR) postrhinal cortex; (PER) perirhinal cortex; (A) amygdala.

Figure 6.

The Type II contextual conditional discrimination employed by Dumont et al. (2007). When the goal boxes are at one end of the rectangular platform, the box covered with the black rectangle is correct (+) and the box covered with the white triangle is incorrect (−). This contingency is reversed when the goal boxes are at the other end. The various features surrounding the platform represent distal cues. This problem, unlike the Type I problem, cannot be solved if the hippocampal formation is damaged.

Figure 7.

The pattern completion and pattern separation processes in the context of Teyler and DiScenna's (1986) indexing theory. Pattern completion: (A) A set of neocortical patterns activated by a particular experience projects to the hippocampal formation and activates a unique set of synapses. The memory for the experiences is stored as strengthened connections among those hippocampal synapses activated by the input pattern (this is the index). (B) A subset of the initial input pattern can activate the index. (C) When this occurs, output from the hippocampal formation projects back to the neocortex to activate the entire pattern. Pattern separation: The hippocampal formation supports pattern separation by creating separate indices to similar input patterns. Note that two similar input patterns (ABCD and CDEF) converge on different representational units in the lower level that represents the hippocampal formation. In contrast, these two patterns would not be separated in the neocortex, so it would have trouble keeping these patterns separated.