We examine two different descriptions of the behavioral functions of the hippocampal system. One emphasizes spatially organized behaviors, especially those using cognitive maps. The other emphasizes memory, particularly working memory, a short-term memory that requires iexible stimulus-response associations and is highly susceptible to interference. The predictive value of the spatial and memory descriptions were evaluated by testing rats with damage to the hippocampal system in a series of experiments, independently manipulating the spatial and memory characteristics of a behavioral task. No (...) dissociations were found when the spatial characteristics of the stimuli to be remembered were changed; lesions produced a similar deficit in both spatial and nonspatial test procedures, indicating that the hippocampus was similarly involved regardless of the spatial nature of the task. In contrast, a marked dissociation was found when the memory requirements were altered. Rats with lesions were able to perform accurately in tasks that could be solved exclusively on the basis of reference memory. They performed at chance levels and showed no signs of recovery even with extensive postoperative training in tasks that required working memory. In one experiment all the characteristics of the reference memory and working memory procedures were identical except the type of memory required. Consequently, the behavioral dissociation cannot be explained by differences in attention, motivation, response inhibition, or the type of stimuli to be remembered. As a result of these experiments we propose that the hippocampus is selectively involved in behaviors that require working memory, irrespective of the type of material that is to be processed by that memory. (shrink)

All recent memory theories of hippocampal function have incorporated the idea that the hippocampus is required to process items only of some qualitatively specifiahle kind, and is not required to process items of some complementary set. In contrast, it is now proposed that the hippocampus is needed to process stimuli of all kinds, but only when there is a need to associate those stimuli with other events that are temporally discontiguous. In order to form or use temporally discontiguous (...) associations, it is essential to maintain some memory of the first component until the second component has occurred. When the temporal gap to he spanned is small, and the number of items to be temporarily retained is low, a limited-capacity, short-term store is sufficient to allow associations to be formed. Such a store is presumed to operate in parallel with the hippocampus in normal animals. Hippocampal damage disrupts a much higher-capacity store that has a slower decay rate, and so leaves animals with only a very limited ability to form temporally discontiguous associations. Hippocampal damage, however, is not held to affect the long-term storage of associations of any kind, if they can be formed. Analyses of both new and existing data are presented to show that by classifying tasks in terms of the need to use a temporary memory store to retain temporally discontiguous information one can cut right across existing classifications as well as achieve a better fit to the data. The hippocampus thus seems best described as a high-capacity, intermediate-term memory store. (shrink)

The hippocampal formation is known for its importance in conscious, declarative memory. Here, we report neuroimaging evidence in humans for an additional role of the hippocampal formation in nonconscious memory. We maskedly presented combinations of faces and written professions such that subjects were not aware of them. Nevertheless, the masked presentations activated many of the brain regions that unmasked presentations of these stimuli did. To induce a nonconscious retrieval of the faces and face-associated occupational information, subjects were instructed to view (...) the previously masked faces and to guess the professional category of each person—academic, artist, and workman. Guessing the professional category of previously masked versus new faces activated the left and right hippocampal formation and right perirhinal cortex as well as bilateral fusiform areas and fronto-temporal areas known to mediate the retrieval of semantic information. These activations within the semantic processing system suggest that conceptual knowledge acquired during masking was nonconsciously retrieved. Our data provide clues to an analogous role of the hippocampus in conscious and nonconscious memory. (shrink)

A complex brain network, centered on the hippocampus, supports episodic memories throughout their lifetimes. Classically, upon memory encoding during active behavior, hippocampal activity is dominated by theta oscillations (6-10Hz). During inactivity, hippocampal neurons burst synchronously, constituting sharp waves, which can propagate to other structures, theoretically supporting memory consolidation. This 'two-stage' model has been updated by new data from high-density electrophysiological recordings in animals that shed light on how information is encoded and exchanged between hippocampus, neocortex and subcortical structures (...) such as the striatum. Cell assemblies (tightly related groups of cells) discharge together and synchronize across brain structures orchestrated by theta, sharp waves and slow oscillations, to encode information. This evolving dynamical schema is key to extending our understanding of memory processes. (shrink)

We raise three issues concerning the Eichenbaum, Otto & Cohen (1994) model. (1) We argue against the strict division of labor that Eichenbaum et al. attribute to neocortical and limbic regions. (2) We raise the possibility that the anterior and posterior portions of the hippocampus may be important for different types of information processing. (3) We argue that, rather than reflecting relational processing, different neural responses to “match” and “nonmatch” trials may relate to different required spatial responses.

Various apparently incompatible theories of hippocampal function have been proposed but integration is now needed. It is argued that the involvement of the hippocampus is most clearly seen when the animal needs to extrapolate beyond current sensory information. Such control can involve both the initiation of behaviour in the absence of appropriate sensory input and the inhibition of behaviour that might otherwise be triggered by current sensory input.

This commentary attempts to reconcile the predictions of Aggleton & Brown's theoretical framework with previous findings obtained from experimental tests of laboratory animals with selective hippocampal lesions. Adopting a convergent operations approach, the predictions of the model are also related to human neuroimaging data and to other complementary research perspectives (cognitive, computational, psychopharmacological).

Recent studies of the contribution made by the hippocampus to spatial behavior suggest that it plays a role in integrating and double integrating distance and direction information using cues generated by self-movement. This and other evidence that the hippocampus plays a central role in spatial behavior seems inconsistent with proposals that it is primarily involved in episodic memory.

In recent years there has been a wealth of studies investigating how memories are allocated in the hippocampus. Some of those studies showed that it is possible to manipulate the identity of neurons recruited to represent a given memory without affecting the memory's behavioral expression. Those findings raised questions about how the hippocampus represents memories, with some researchers arguing that hippocampal neurons do not represent fixed stimuli. Herein, an alternative hypothesis is argued. Neurons in high‐order brain regions can (...) be tuned to multiple dimensions, forming complex, abstract representations. It is argued that such complex receptive fields allow those neurons to show some flexibility in their responses while still representing relatively fixed sets of stimuli. Moreover, it is pointed out that changes induced by artificial manipulation of cell assemblies are not completely redundant—the observed behavioral redundancy does not imply cognitive redundancy, as different, but similar, memories may induce the same behavior. (shrink)

A fundamental assumption in Shors & Matzel's target article is that brain activity can be related to the traditional categories of mentalistic psychology. This has led them to make numerous further assumptions that are contradicted by the available evidence.

Theories of spatial cognition are derived from many sources. Psychologists are concerned with determining the features of the mind which, in combination with external inputs, produce our spatialized experience. A review of philosophical and other approaches has convinced us that the brain must come equipped to impose a three-dimensional Euclidean framework on experience – our analysis suggests that object re-identification may require such a framework. We identify this absolute, nonegocentric, spatial framework with a specific neural system centered in the (...) class='Hi'>hippocampus.A consideration of the kinds of behaviours in which such a spatial mapping system would be important is followed by an analysis of the anatomy and physiology of this system, with special emphasis on the place-coded neurons recorded in the hippocampus of freely moving rats. A tentative physiological model for the hippocampal cognitive map is proposed. A review of lesion studies, in tasks as diverse as discrimination learning, avoidance, and extinction, shows that the cognitive map notion can adequately explain much of the data.The model is extended to humans by the assumption that spatial maps are built in one hemisphere, semantic maps in the other. The latter provide a semantic deep structure within which discourse comprehension and production can be achieved. Evidence from the study of amnesic patients, briefly reviewed, is consistent with this extension. (shrink)

Theories of superior collicular and hippocampal function have remarkable similarities. Both structures have been repeatedly implicated in spatial and attentional behaviour and in inhibitory control of locomotion. Moreover, they share certain electrophysiological properties in their single unit responses and in the synchronous appearance and disappearance of slow wave activity. Both are phylogenetically old and the colliculus projects strongly to brainstem nuclei instrumental in the generation of theta rhythm in the hippocampal EECOn the other hand, close inspection of behavioural and electrophysiological (...) data reveals disparities. In particular, hippocampal processing mainly concerns stimulus ambiguity, contextual significance, and spatial relations or other subtle, higher order characteristics. This requires the use of largely preprocessed sensory information and mediation of poststimulus investigation. Although collicular activity must also be integrated with that of “higher” centres, its primary role in attention is more “peripheral” and specific in controlling orienting/localisation via eye and body movements toward egocentrically labelled spatial positions. In addition, the colliculus may exert a nonspecific influence in alerting higher centres to the imminence of information potentially worthy of focal attention. Nevertheless, it is noteworthy that collicular and hippocampal lesions produce deficits on similar tasks, although the type of deficit is usually different in each case. Functional overlap between hippocampus and colliculus is virtually certain vis-à-vis stimulus sampling, for example in the acquisition of information via vibrissal movements and visual scanning. In addition, insofar as stimulus significance is a factor in collicular orienting mechanisms, the hippocampus — cingulate – cortex — colliculus pathway may play a significant role, modulating collicular responsiveness and thus ensuring an attentional strategy appropriate to current requirements. A tentative “reciprocal loop” model is proposed which bridges physiological and behavioural levels of analysis and which would account for the observed degree and nature of functional overlap between the superior colliculus and hippocampus. (shrink)

Though hippocampal volume reduction is a pathological hallmark of schizophrenia, the molecular pathway responsible for this degeneration remains unknown. Recent reports have suggested the potential role of impaired blood-brain barrier function in schizophrenia pathogenesis. However, direct evidence demonstrating an impaired BBB function is missing. In this preliminary study, we used immunohistochemistry and serum immunoglobulin G antibodies to investigate the state of BBB function in formalin-fixed postmortem samples from the hippocampus and surrounding temporal cortex of patients with schizophrenia and controls (...) without schizophrenia matched for age, sex, and race. Since a functional BBB prevents the extravasation of IgGs, detection of IgGs in the parenchyma is used as direct evidence of BBB breakdown. We also developed a semi-quantitative approach to quantify the extent of IgG leak and therein BBB breach. Analysis of our immunohistochemistry data demonstrated a significantly higher incidence of IgG leak in patients with schizophrenia compared to controls. Further, BBB permeability was significantly higher in advanced-age patients with schizophrenia than both advanced-age controls and middle-aged patients with schizophrenia. Male patients with schizophrenia also demonstrated a significant increase in IgG permeability compared to control males. Interestingly, the extravasated IgGs also demonstrated selective immunoreactivity for neurons. Based on these observations, we suggest that BBB dysfunction and IgG autoantibodies could be two key missing pathoetiological links underwriting schizophrenia hippocampal damage. (shrink)

Aboitiz et al. suggest that the mammalian isocortex is derived from the dorsal cortex of reptiles and birds, and that there has been a major divergence in the connectivity patterns (and hence function) of the mammalian and reptilian/avian hippocampus. There is considerable evidence to suggest, however, that the avian hippocampus serves the exact same function as the mammalian hippocampus.

Aggleton & Brown have built a convincing case that hippocampus-related circuits may be involved in thalamic amnesia. It remains to be established, however, that their model represents a distinct neurological system, that the distinction between recall and familiarity captures the roles of these pathways in episodic memory, or that there are no other systems that contribute to the signs of amnesia associated with thalamic disease.

An alternative to Aggleton & Brown's interpretation is presented suggesting that the perirhinal cortex and hippocampus mediate different attribute information, but use the same processes, supporting the idea of parallel processing based on attribute (visual object and spatial location) rather than process characteristics (item recognition and familiarity).

The proposal that the hippocampus is important for the encoding of episodic information, but not familiarity-based recognition, is incompatible with the available data. An alternative way to think about functional specialization within the medial temporal lobe memory system is suggested, based on neuroanatomy.