Hippocampal place cells, context, and episodic memory

Abstract

ABSTRACT:Although most observers agree that the hippocampus has a critical role in learning and memory, there remains considerable debate about the precise functional contribution of the hippocampus to these processes. Two of the most influential accounts hold that the primary function of the hippocampus is to generate cognitive maps and to mediate episodic memory processes. The well-documented spatial firing patterns (place fields) of hippocampal neurons in rodents, along with the spatial learning impairments observed with hippocampal damage support the cognitive mapping hypothesis. The amnesia for personally experienced events seen in humans with hippocampal damage and the data of animal models, which show severe memory deficits associated with hippocampal lesions, support the episodic memory account. Although an extensive literature supports each of these hypotheses, a specific contribution of place cells to episodic memory has not been clearly demonstrated. Recent data from our laboratory, together with previous findings, indicate that hippocampal place fields and neuronal responses to task-relevant stimuli are highly sensitive to the context, even when the contexts are defined by abstract task demands rather than the spatial geometry of the environment. On the basis of these findings, it is proposed that place fields reflect a more general context processing function of the hippocampus. Hippocampal context representations could serve to differentiate contexts and prime the relevant memories and behaviors. Since episodic memories, by definition, include information about the time and place where the episode occurred, contextual information is a necessary prerequisite for any episodic memory. Thus, place fields contribute importantly to episodic memory as part of the needed context representations. Additionally, recent findings indicate that hippocampal neurons differentiate contexts at progressively finer levels of detail, suggesting a hierarchical coding scheme which, if combined with temporal information, could provide a means of differentiating memory episodes. V V C 2006 Wiley-Liss, Inc.

Hippocampal and neocortical interactions during context discrimination: Electrophysiological evidence from the rat

“…Shors and Matzel, 1997). These results not only support the hypothesis that hippocampus processes context information, but more specifically, they indicate that hippocampus plays a particularly salient role in the discrimination of meaningful contexts (Smith and Mizumori, 2006a).…”

“…While significant evidence supporting the existence of these operations in hippocampus can be derived from single unit recordings in behaving rats, it remains a significant challenge to understand how context processing theories of hippocampus account for the varied hippocampal place cell responses that have been reported. The following description of a context discrimination hypothesis (CDH; Smith and Mizumori, 2006a;Mizumori, 2007) provides a theoretical framework to account for a significant amount of the place cell findings, as well as to provide a link to current ideas about the specific role of the hippocampus in learning and episodic memory (Tulving, 2002). While many features of this hypothesis build on concepts discussed by other investigators (as pointed out below), its consideration here provides an opportunity to elaborate specifically on the functional networks that should exist as part of hippocampal neural organization.…”

Dopamine modulates synaptic plasticity in dendrites of rat and human dentate granule cells

“…Thus, the TBP protocol here was designed to mimic the physiological activation of a place cell (1-3) and the theta oscillations from the entorhinal cortex that occur during exploratory behavior (2,3). Although we did not examine the LPP here, because D1Rs are distributed uniformly along the dendritic tree of DGCs (9), and VTA dopamine fibers broadly innervate the dentate molecular layer, we anticipate that a similar mechanism could well also facilitate plasticity in the LPP, although this remains to be tested.…”

“…A s an animal explores a specific location, place cells in the dentate gyrus (DG) of the hippocampus fire bursts of action potentials (APs) (1) that can result in the formation of a new, long-term contextual memory (2). This is part of the "pattern separation" mechanism, whereby only a small population of dentate granule cells (DGCs) become very active and pass on the incoming cortical input to be later represented or "completed," in the downstream CA3 network (3).…”

A single low dose of valproic acid in late prenatal life alters postnatal behavior and glutamic acid decarboxylase levels in the mouse

“…In particular, the hippocampus is thought to regulate processing of contextual cues [63,64]. Thus "non-selective" associative learning by VPA exposed animals may be underpinned by some "disconnect" between amygdala and hippocampus hubs involved in stimulus processing.…”