Review
Regional dissociations within the hippocampus—memory and anxiety

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Abstract

The amnestic effects of hippocampal lesions are well documented, leading to numerous memory-based theories of hippocampal function. It is debatable, however, whether any one of these theories can satisfactorily account for all the consequences of hippocampal damage: Hippocampal lesions also result in behavioural disinhibition and reduced anxiety. A growing number of studies now suggest that these diverse behavioural effects may be associated with different hippocampal subregions. There is evidence for at least two distinct functional domains, although recent neuroanatomical studies suggest this may be an underestimate. Selective lesion studies show that the hippocampus is functionally subdivided along the septotemporal axis into dorsal and ventral regions, each associated with a distinct set of behaviours. Dorsal hippocampus has a preferential role in certain forms of learning and memory, notably spatial learning, but ventral hippocampus may have a preferential role in brain processes associated with anxiety-related behaviours. The latter's role in emotional processing is also distinct from that of the amygdala, which is associated specifically with fear. Gray and McNaughton's theory can in principle incorporate these apparently distinct hippocampal functions, and provides a plausible unitary account for the multiple facets of hippocampal function.

Section snippets

Preferentially dorsal hippocampus-dependent functions

An opportunity to reconcile these accounts of hippocampal function has arrived with the demonstration that lesions of different hippocampal subregions have distinct and dissociable behavioural effects. A number of early behavioural experiments [60], [92], [121], [119] coupled with anatomical studies demonstrating clear differences in afferent and efferent connectivity along the septotemporal extent of the hippocampus [118], [123], [133], had hinted at potential differences between dorsal and

Preferentially ventral hippocampus-dependent functions

Identification of clearly dorsal hippocampus-dependent functions (that are largely ventral hippocampus independent) raises the intriguing question as to whether the ventral hippocampus might likewise be preferentially involved in a particular subset of hippocampus-dependent behaviours [59], [88]. As was outlined above, the preferential involvement of the dorsal hippocampus in spatial information processing is entirely consistent with its known anatomical connectivity-dorsal hippocampus receives

Partial hippocampal lesion effects in freezing paradigms and the watermaze

There is a widely held notion that spatial learning, as exemplified by tasks such as the Morris watermaze, and contextual fear conditioning are essentially different manifestations of the same basic underlying process [80], [93], [97], [115], [122]. Such a line of thought is tempting because there is an intuitive similarity between these spatial and contextual forms of learning in that both are likely to involve processing, perhaps integrating, complex stimuli which are often large [27],

Partial hippocampal lesion effects on unconditioned ethologically based tests of anxiety

The possibility that the ventral hippocampus may have a specialised role in fear or anxiety related behaviours has also recently been examined using a series of unconditioned anxiety tests [81]. This study had two goals. First, it extended the comparison of the effect of dorsal and ventral hippocampal lesions to examine the generality of the inferences derived from freezing studies. Second, a group of animals with cytotoxic lesions of the amygdalar complex (intended to include all the major

The roles of the ventral hippocampus and amygdala in anxiety-related processes

Direct comparison between the effects of amygdala lesions and ventral hippocampal lesions revealed a number of important and notable distinctions. Amygdala lesions had no effect on the successive alleys test, a result which is consistent with several previous demonstrations that these lesions, in contrast to hippocampal damage, have no effect on performance on the elevated plus maze [37], [70], [120], [125], [126], [127]. Amygdala lesions also had no significant effect on social interaction (to

Conclusions

The results we have reviewed support the idea that fear and anxiety are distinct, emotional entities with separate underlying neural substrates. Furthermore, they support Gray and McNaughton's [56] distinction between the contributions of the hippocampus and amygdala to emotional behaviour, suggesting differential roles for these structures in anxiety and fear respectively. The two brain systems are of course likely to be highly interactive. These distinctions, and their respective places

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    Present address: Department of Neuroscience, University of Edinburgh, 1 George Square, Edinburgh EH8 9JZ, Scotland, UK.

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