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The Hippocampus and Memory: Insights from Spatial Processing

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The Hippocampus and Memory: Insights from Spatial Processing REVIEWS MEMORY SYSTEMS The hippocampus and memory: insights from spatial processing Chris M. Bird and Neil Burgess 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. Short-term memory Lying deep in the medial temporal lobes, the hippo- predictions about the effects of hippocampal damage or to The conscious retention of campal formation is one of the most studied neuronal identify the computations that are performed in the hip- information over a few systems in the brain1 (FIG. 1). Researchers seeking to pocampus. More detailed theories do make predictions seconds, often through active understand the function of the hippocampus have taken as to the effects of selective hippocampal damage, but the maintenance (rehearsal). When their inspiration from a wide range of sources. Some experimental data are equivocal, as summarized below. the information held in short- term memory is manipulated, have started with the devastating effects on memory Theories that focus on a particular area of cognition can this is often referred to as that follow bilateral medial temporal lobe damage and link neuronal firing to some limited aspects of behaviour working memory. the similar, but milder, effects of selective damage to the but can be hard to generalize to other situations. hippocampus. In general, such patients are impaired in In parallel with the experiment-driven development Priming A behavioural change that is acquiring new, consciously accessible (that is, explicit) of these theories, computational models of hippocampal manifested in the speed or memories, whereas short-term memory, priming, procedural function have also been proposed — on more theoretical accuracy with which a stimulus learning and some remote memories that were acquired grounds. This approach enables hypotheses regarding is processed following prior well before the lesion are preserved2–6 (see FIG. 2; the operation of the hippocampus and related areas to exposure to the same or a although see below for recent evidence that the hippo- be constrained by physiological data. Computational similar stimulus. campus subserves some aspects of short-term memory). modelling of the hippocampus and its interaction with 16,17 Procedural learning The pattern of spared and impaired cognitive processes surrounding neocortical areas was started by Marr . The unconscious learning of a in patients with hippocampal damage, combined with In Marr’s model, and in important work that extended skill, such as a series of actions results from animal models of amnesia, has lead to the or clarified it18–22, a sparse hippocampal representation or perceptual processing 7,8 functions (for example, learning Declarative Theory of hippocampal function . Others of an event is rapidly encoded through the modification of to ride a bike), which typically have sought more specific characterizations of hippo- recurrent connections in area CA3 of the hippocampus. results in increased speed or campal function, drawing on experimental data from This representation affords subsequent retrieval by an accuracy with repetition. animals and humans. This has lead to, for example, the incomplete cue through pattern completion, and thence Multiple-Trace Theory9,10, the Dual-Process Theory11 reinstatement of the full representation of the event in and the Relational Theory12–14. Lastly, some researchers disparate neocortical areas. Marr’s model predicts that have focused on building a neural-level understanding the hippocampus is required for the initial encoding of Institute of Cognitive Neuroscience and of hippocampal function in a specific cognitive domain; multi-modal information that is represented in cortical Department of Anatomy, examples of this approach include the Cognitive-Map areas: it provides a ‘convergence zone’ to mediate these University College London, Theory15. These different theories are briefly described associations23. London, WC1N 3AR, UK. in BOX 1. In this Review we briefly summarize the current state e-mails: [email protected]; Of course, all of these approaches have their merits of the debate regarding the role of the human hippocam- [email protected] doi:10.1038/nrn2335 and drawbacks. The Declarative Theory is consistent pus in long-term memory. We then describe a model of Published online with the bulk of human neuropsychological data, but hippocampal function that has similarities with Marr’s 13 February 2008 it lacks the specificity that is necessary to make novel model but specifically focuses on the spatial domain, 182 | marcH 2008 | VolUME 9 www.nature.com/reviews/neuro © 2008 Nature Publishing Group REVIEWS a Anterior thalamic Cingulate gyrus in which the neuronal representations of memory have nuclei been well studied. Some of the controversies concerning Fornix the role of the hippocampus in long-term memory are Basal forebrain then revisited in light of this model. We then discuss the model’s implications for hippocampal processing outside Retrosplenial Amygdala cortex the domain of long-term memory. Lastly, we highlight some of the aspects of cognitive processing that are not Mammilary addressed by the model but that are nevertheless thought body to be underpinned by the hippocampus. Parahippocampal Perirhinal cortex Episodic and semantic memory cortex A striking feature of the memory problems that fol- low hippocampal damage is an inability to remember Entorhinal Hippocampus cortex recent events. Nevertheless, patients with hippocampal damage typically have a normal vocabulary, and their general knowledge of facts remains intact. Interestingly, b Thalamus Hypothalamus Basal forebrain the opposite pattern of memory loss is associated with a specific form of neurodegenerative disease known as Mammiliary MDTN ATN Septal ‘semantic dementia’: here, recent events are retrieved bodies nuclei accurately whereas knowledge of word meanings and facts is dramatically impaired24. The type of memory that involves personally experienced events was termed Amygdala ‘episodic memory’ by Tulving, who contrasted it with Fornix other aspects of declarative memory, such as knowl- edge of facts in the absence of memory for the context Hippocampus Subiculum in which they were learned (‘semantic memory’) or Presubiculum context-independent recognition of stimuli based on a feeling of familiarity25,26. Entorhinal The Declarative Theory explains these dissociations cortex in terms of the age of the memories. Based on clinical observations2 and theoretical ideas17, it proposes that older memories become ‘consolidated’ to neocortical Perirhinal Parahippocampal areas outside of the medial temporal lobe. According cortex cortex to this theory, recently acquired episodic memories are vulnerable to hippocampal damage, whereas facts that Cing were learnt long ago are not. Similarly, the Declarative 46 11/12 Insular gyrus Theory predicts that hippocampal damage impairs the TE V4 7a/ TEO cortex LIP acquisition of new knowledge but leaves remote episodic 13 RSp cortex memories intact. Nonetheless, a compelling alternative explanation for these data, as proposed by the Multiple- Frontal lobe Temporal lobe Parietal lobe Trace Theory, is that both recent and remote episodic Figure 1 | The hippocampus and its connections. a | The hippocampus lies in the memories depend on the hippocampus. According medial temporal lobes, surrounded by the entorhinal, parahippocampalNature Revie wsand | Neurperirhinaloscienc e to this theory, the hippocampus and adjacent regions cortices. It is part of Papez’s circuit, and so is connected to several subcortical and (the perirhinal and parahippocampal cortices) con- cortical structures, such as the anterior thalamic nuclei (ATN), the mammillary bodies, the septal nuclei of the basal forebrain, the retrosplenial cortex and the parahippocampal nect and store memory traces of the information that cortex. b | Cortical and subcortical connections of the hippocampus. Subcortical represents an event and is stored in the neocortex. Each connections are indicated by red lines; cortical connections are indicated by black lines. time the memory of an event is retrieved, a new hip- The thickness of the black lines approximates to the strength of the connections. Most of pocampally mediated trace is created, such that older the hippocampus’s neocortical inputs come from the perirhinal and parahippocampal memories are represented by more traces than new cortices, through the entorhinal cortex, and most of its neocortical output is through the ones and are therefore less susceptible to disruption. In subiculum, which also projects back to the entorhinal cortex. Both the perirhinal cortex addition, as more traces of the same event are formed, and the parahippocampal cortex lie at the end of the ventral visual processing (‘what’) the information belonging to that event, which is stored stream. The perirhinal cortex is crucial for the representation of complex objects, in the neocortex, becomes integrated with pre-existing
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