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This chapter examines how space is represented in the primate hippocampus, how this is related to the memory and spatial functions performed by the hippocampus, and how the hippocampus performs these functions. It is shown that in the primate hippocampal spatial-view cells could be involved in arbitrary associations with the objects and rewards which are presented at particular viewed locations. A new investigation of object-place recall memory is described, which shows some of the representations that become active within the hippocampus when places are recalled from objects.

This chapter reviews relevant data on the relationships between place cell firing and animals' spatial behavior. Evidence suggests that there is an interaction between place cells and behavior. Two complementary aspects of this interaction have emerged from these studies — namely, that place cells guide spatial behavior and, conversely, that behavior influences place cell firing.

This chapter reviews attempts to determine how activity of neurons in the place system — place cells and the more recently discovered head direction and entorhinal grid cells — relates to what the animal “knows”, as manifest by how it behaves. Beginning with O'Keefe and Nadel's cognitive map hypothesis, the chapter explores the extent to which behavioral experiments have supported this idea, before turning to the question of how, if at all, these neurons contribute to episodic memory. It argues that while data suggesting a role for place cells in encoding transient events are scarce, data suggesting that cells may encode the spatial-contextual scaffolding for the attachment of episodic memory are plentiful and plausible.

The evidence on spatial and nonspatial neural firing patterns of hippocampal neurons suggests that the hippocampus encodes a broad range of new information within a “memory space”. Hippocampal place cells demonstrate location specific firing, but these spatial firing patterns do not reflect a straightforward encoding of the global topology of the environment. Rather, spatial firing patterns of hippocampal neurons include substantial information about nonspatial stimuli and ongoing behavior, including ongoing behavioral actions and behavioral demands of an ongoing task. In addition, hippocampal encode nonspatial stimuli and behaviors in situations where distinctive events are distributed around the environment. Both the spatial and nonspatial firing properties of hippocampal neurons emphasize conjunctions or relations among task elements, and include a very broad range of stimuli and behaviors.

This chapter reviews current knowledge about spatial representations in medial entorhinal cortex (MEC), its possible role in navigation, and how cell ensembles in MEC might contribute to the spatial component of hippocampal place cell representations. The discovery of a metric representation of self-location in MEC suggests that the primary function of the hippocampus is not the dynamic computation of location. Although the animal's position can be predicted from the collective firing of grid cell ensembles, it remains to be determined whether readout occurs within the entorhinal cortex or in one or several of its hippocampal or parahippocampal target structures. The contextual specificity of hippocampal representations suggests that during encoding, the hippocampus associates input from the self-motion-based coordinate system in MEC with other contextual information such as information from lateral entorhinal cortex (LEC). The possible recoding of spatial information from a positional code in MEC onto statistically independent, context-sensitive cell ensembles in high-capacity networks of the hippocampus is probably crucial for the successful storage of episodic memory.

This chapter begins with a discussion of the idea of the hippocampus is a cognitive map. It then discusses the limbic system, which contains several distinct cell types that show environmentally invariant spatial firing properties; followed by path integration in the hippocampus and other limbic regions. The significance of the hippocampal “place cell” firing fields if the hippocampus does not constitute the cognitive map is considered.

This chapter covers a number of topics including systems-level functions of the hippocampus, head direction cells and perirhinal cortex, recognition memory, and long-term familiarity memory. A theory of the operation of hippocampal circuitry as a memory system is described.

This chapter reviews current knowledge about aged neural ensembles in the hippocampus and how alterations in the dynamics of these circuits are linked to memory decline. Topics discussed include fundamental properties of place cells in young and old rats, advanced age and the dynamic properties of hippocampal place cells, and memory decline. It is shown that old rats have notable differences in the dynamic properties of CA1 place fields, and several of these differences correspond with observed age-associated behavioral deficits. Aged rats fail to show experience-dependent place field expansion plasticity to the same extent as young rats. Between episodes of experience in a single environment, aged rats are also impaired at maintaining stable spatial representations in the CA1 subregion of the hippocampus. This observation is consistent with the finding that old rats exhibit impaired performance on tasks requiring the solution of an allocentric spatial reference frame.

Single-cell recording from hippocampal place cells has enabled the development of detailed models of spatial memory. This chapter focuses on the BVC model, which predicts a role for the hippocampus in the construction of rich and dynamic first-person perspective imagery. Episodic memory is simply one form of imagery — the reconstruction of previously experienced events. The ability to construct such images gives rise to feelings of recollection or re-experiencing the events. The model also predicts a role for the hippocampus in some forms of spatial working memory and the ability to construct novel images, consistent with recent experimental data.

This chapter summarizes and extends arguments made in recent reviews that challenge the notion that hippocampal cells are “place cells”, and suggests instead that hippocampal neuronal activity should be examined with regard to memory processing functions of the hippocampus. It begins by reconsidering the case for a selective role of the hippocampus in spatial processing and the phenomenon of place cells. It then outlines an alternative hypothesis about hippocampal function in memory and offers a reconciliation of the spatial and memory processing views of hippocampal neuronal activity.

This chapter reviews what is known about place cells. Under normal circumstances, the location in which a place cell fires — its place field — is anchored to the visual landmarks within the environment. However, place cells also fire in the dark, and evidence shows that their firing also reflects path integration. Place cells are sensitive to boundaries in the environment, and the boundary-vector model developed by Neil Burgess and colleagues posits that place cells are the product of boundary cells tuned to walls or boundaries in different directions. Place cell firing is also modulated by the behaviour of the animal, and can reflect its intended destination. Place cell-like activity is found in non-human primates and in humans. Imaging studies in humans have provided some support for a role of the hippocampus is navigation and cognitive mapping, and have also highlighted a contribution from the parahippocampal gyrus.

This chapter shows that place cells can provide a view into the individual differences associated with cognitive aging. For instance, they illustrate that at least with aging, memory success requires a flexible hippocampus, whereas memory failures are characterized by an inflexible hippocampus poorly prepared for making new memories. With continued development of new behavioral tasks, especially those suitable for genetically engineered mice to investigate molecular mechanisms of memory, place cells will provide an important and insightful tool.

The relationship between context-dependent hippocampal activity and tasks that are hippocampus dependent is not clear-cut. Although in some hippocampus-dependent tasks context-dependent place field firing is seen, in others it is not. Furthermore, in some tasks that don't require a hippocampus, context-dependent activity is observed. This chapter reviews these three patterns of results and identifies the task characteristics that yield context-dependent place cell firing, as well as the characteristics of tasks that require the hippocampus. It is argued that at the very least, structures outside the hippocampus are capable of mediating context discrimination sufficient to support some kinds of context-dependent behaviors. This suggests that the hippocampus is one component of a network of structures that together allow context discrimination and mediate the performance of context-dependent memory tasks.

Along with place cells, the hippocampal theta rhythm is one of the most predominant and well-studied physiological patterns in the hippocampal literature. This chapter outlines the major behavioral correlates of theta rhythm, particularly pertaining to learning and memory, and then discusses the relationship between theta rhythm and the activity of individual neurons (including place cells) in hippocampus. Computational models that have been used to link learning and memory functions to theta rhythm and theta-related hippocampal unit firing are reviewed to generate hypotheses for future experimental studies.

A central theme in the study of animal navigation has been the extent to which such navigation requires the formation of an internal representation of space, the so-called “cognitive map.” Although its properties remain disputed, it is now generally accepted that a map-like representation exists in the brain, and neurobiological studies, conducted in tandem with behavioral investigations, have done much to elucidate the neural substrate of the map as it operates in two dimensions. However, to date little is known about how the map encodes real-world, three-dimensional space. Using recent neurobiological and behavioral findings, this issue is explored here. It is argued that the navigational problems in three dimensions are qualitatively as well as quantitatively different from those in two dimensions, and evidence suggests that, perhaps for this reason, horizontal and vertical space are processed separately in the vertebrate brain. The possible adaptive consequences of such an anisotropic encoding scheme are outlined.

This chapter describes evidence that the place cells are themselves also responsive to nongeometric stimuli, such as the colour and odour of an environment — stimuli that give an environment its quality, or character. It also proposes that the stimuli act by somehow selecting which (of possibly several sets of) spatial inputs will drive the cell. In addition, it explores the possible nature of representation of spatial context, including how it may develop with experience. Moreover, it evaluates how the contextual inputs interact with spatial inputs onto place cells, and what is the nature of these contextual inputs. In general, the data confirm the hypothesis that a function of the hippocampus is to assemble a configural representation of spatial context, for the purposes of enabling context-dependent behaviours and learning processes.

The hippocampal system provides a beautiful example of how different classes of neuronal network in the brain work together as a system to implement episodic memory, the memory for particular recent events. The hippocampus contains spatial view neurons in primates including humans, which provide a representation of locations in viewed space. These representations can be combined with object and temporal representations to provide an episodic memory about what happened where and when. A key part of the system is the CA3 system with its recurrent collateral connections that provide a single attractor network for these associations to be learned. The computational generation of time, encoded by time cells in the hippocampus, is described, and this leads to a theory of hippocampal replay and reverse replay. The computational operation of a key part of the architecture, the recall of memories to the neocortex, is described.

This chapter takes an analytical approach to the construction of place fields in order to explore what information the cells receive and from which areas, and how they piece this together to produce the phenomena seen in the laboratory. It concentrates on place cells in rodents. First, it briefly sketches key aspects of hippocampal formation connectivity in order to ground discussion in later sections. It then surveys the types of spatial information required by cognitive map theory, and their instantiation in the hippocampal formation. In addition, recent evidence relevant to encoding of distance and speed is considered. It also describes the degree to which experience-dependent plasticity is required to explain hippocampal place cell characteristics and functioning, and outlines data showing long-term plasticity in place cells, suggesting they form a substrate for incidental environmental learning. Some consideration is given to the nature of the plasticity involved. Furthermore, it addresses the aspects of the relationship between the hippocampal formation and behaviour in the spatial domain.