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The hippocampus and memory: insights from spatial processing

Key Points

  • Damage to the hippocampus in humans can cause profound impairments in long-term episodic memory, but the precise functional contribution of the hippocampus remains the subject of several competing theories.

  • Electrophysiological studies in rodents have characterized the firing properties of 'place cells' in the hippocampus in great detail. Place cells appear to represent where an animal 'thinks' it is located in an environment, relative to environmental boundaries. Acting cooperatively, place cells encode specific environments, performing both pattern completion and pattern separation.

  • A new model of hippocampal processing that is driven by the properties of place cells (the BBB model) provides an alternative to existing psychological theories, at least in the spatial domain. The BBB model proposes that the hippocampus is needed to impose a location from which to retrieve and construct a coherent mental image of an environment. This mental image supports the online maintenance and manipulation of representations of the locations of objects and features in an environment.

  • The model suggests that episodic memory will always be hippocampus-dependent if it is associated with rich mental imagery of an environment. Other sophisticated long-term spatial (and non-spatial) representations can be acquired, stored and retrieved independent of the hippocampus. However, the hippocampus is often needed to mediate behaviours that allow such learning to take place (such as when learning a new route).

  • The BBB model further suggests that the hippocampus is required for both short-term and long-term memory for some types of information, for imagining complex visual scenes (be they real or fictitious), and more for the recognition of scenes than faces. Recent experimental evidence from studies of the effects of damage to the hippocampus in humans supports all three of these proposals.

  • Hippocampal processing beyond the spatial domain cannot be explained by the BBB model, but several theoretical positions have been advanced to address the broader role of the hippocampus in mnemonic processing.

Abstract

The hippocampus appears to be crucial for long-term episodic memory, yet its precise role remains elusive. Electrophysiological studies in rodents offer a useful starting point for developing models of hippocampal processing in the spatial domain. Here we review one such model that points to an essential role for the hippocampus in the construction of mental images. We explain how this neural-level mechanistic account addresses some of the current controversies in the field, such as the role of the hippocampus in imagery and short-term memory, and discuss its broader implications for the neural bases of episodic memory.

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Figure 1: The hippocampus and its connections.
Figure 2: The traditional taxonomy of memory systems.
Figure 3: Stimuli used to investigate the role of the hippocampus in perception and short-term memory.

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Acknowledgements

We gratefully acknowledge the support of the Medical Research Council UK, the Biotechnology and Biological Sciences Research Council, UK, and a European Union Wayfinding Grant. We thank T. Shallice, J. O'Keefe, and three anonymous referees for their invaluable help in the preparation of this manuscript.

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Glossary

Short-term memory

The conscious retention of information over a few seconds, often through active maintenance (rehearsal). When the information held in short-term memory is manipulated, this is often referred to as working memory.

Priming

A behavioural change that is manifested in the speed or accuracy with which a stimulus is processed following prior exposure to the same or a similar stimulus.

Procedural learning

The unconscious learning of a skill, such as a series of actions or perceptual processing functions (for example, learning to ride a bike), which typically results in increased speed or accuracy with repetition.

Recurrent connections

The extensive reciprocal connections between principal CA3 neurons. This unusual neural architecture might provide a substrate for the implementation of an attractor network that supports associative memory.

Pattern completion

A process by which a stored neural representation is reactivated by a cue that consists of a subset of that representation.

Path integration

The ability to keep track of the start position of a trajectory by integrating the movements made along the path.

Pattern separation

A process by which small differences in patterns of input activity are amplified as they propagate through a network. This creates distinct representations.

Attractor network

Neural networks that have one or more stable 'states' (that is, patterns of firing across neurons). The stable states are determined by the strengths of the recurrent connections between the neurons in the network. Depending on the initial conditions, the network will end up in one of the stable states. This can allow pattern completion to occur.

Papez's circuit

A network of limbic brain structures that was originally thought to subserve emotional processing. These structures include the cingulate cortex, the hippocampus, the mammillary bodies, the anterior thalamus and the projections between these areas, such as the fornix.

Saccade

Quick, simultaneous movements of both eyes in the same direction, allowing one to fixate rapidly on elements of a visual scene or a passage of text.

Receiver operating characteristics

(ROCs). An ROC describes the relationship between hits and false alarms across varying confidence levels. Yonelinas has argued that the shape of the ROC varies according to the independent contributions of recollection and familiarity to performance on a memory task.

Sensory buffers

Dedicated neocortical systems that (independently) support the short-term maintenance of sensory, motor, linguistic or other information.

Unitized stimuli

Uni-modal elements of an event that, according to dual-process and relational theories, can be represented and subsequently recognized by brain regions outside of the hippocampus.

Theta frequency range

Rhythmic activity (4–12 Hz) detected in the local field potential or by electroencephalogram. This rhythm is particularly prominent in the hippocampus of rats during locomotion and has recently been related to mnemonic processing in both rats and humans.

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Bird, C., Burgess, N. The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9, 182–194 (2008). https://doi.org/10.1038/nrn2335

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