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.Everything we experience happens somewhere. The term ''context'' is often used to denote this ''somewhere.'' In the analysis of learning and memory, the context is like the setting for a stage play (Medin and Reynolds 1985). It provides the background for the real action in the drama-the main events. More importantly, as a consequence of learning and memory processes, the context often helps to select appropriate behaviors and determine the explicit and implicit content of our thoughts. Thus, it is not surprising that psychologists have a long-standing empirical and theoretical interest in understanding just what makes up a representation of context and how context representations interact with the main events of our lives to influence our behavior (see Balsam and Tomie 1985).More recently, neurobiologists have increased their interest in the problem of linking context representations and functions to brain systems. The hippocampal formation emerged quite early as a major focal point among many researchers. As a result, there is a substantial literature linking the hippocampal formation and context. However, on the surface, this research yields a dismaying set of conflicting results, with many findings that the hippocampal formation plays a critical role in supporting the influence of context on memory and behavior and many other findings that it does not.The goal of this article is to bring some clarity and order to this state of affairs. I start by providing a working definition of ''context'' that implicitly underpins its experimental analysis. I then describe several different functions of context that have been studied in the laboratory and are assumed to be theoretically important. I then introduce and build on a dual-process theory of context representations that was put forth several years ago by Lynn Nadel, Jeffrey Willner, and colleague...

Systemic Administration of γ-Hydroxybutyric Acid in Adolescent Rat Impairs Contextual Fear Conditioning, But Not Cued Conditioning

“…Contextual fear acquisition involves configural or spatial learning [47], and is mediated by the hippocampus [43]. It is well established that fear conditioning to a target tone is mediated by the amygdala [30,33], and conditioning to context is primarily mediated by the hippocampus [44,45,46,49,67]. Thus, the present data supports the hypothesis that GHB in adolescent rats disrupts hippocampal functions.…”

“…Alcohol has been reported to disrupt contextual freezing in young animals, and this alcohol-induced memory deficit is associated with significant CA1 pyramidal neuronal loss [6,35,59]. Some other brain areas that are thought to support contextual fear conditioning include parahippocampal structures [18,46], medial prefrontal cortex [20], medial geniculate nucleus [31], and cerebellum [48].…”

Object/context-specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats

“…Our finding that the selective loss of DG granule cells produces a deficit in object memory only when the rat must remember the context in which the object had been previously encountered adds to a converging body of evidence that suggests the hippocampus is essential in storing and retrieving certain types of context memories (Rudy 2009). Specifically, we show that hippocampal granule cells are necessary for supporting associations between objects and contexts.…”

When Is the Hippocampus Involved in Recognition Memory?

“…Thus, in those studies that show an involvement of the hippocampus in object recognition, the presence of two different objects in the sample phase might create additional contextual cues or object-object associations that are themselves vulnerable to hippocampal damage. Indeed, previous studies have suggested that the hippocampus can play a role in object recognition if such cues are present (Rudy, 2009;Oliveira et al, 2010). The demonstration that disconnection of the hippocampus from either the perirhinal or medial prefrontal cortex produces significant impairments in the object-in-place task is an important addition to our knowledge of which regions interact during recognition memory tasks involving the integration of object and spatial information.…”