The authors draw together the results of a series of detailed computational studies and show how they are contributing to the development of a theory of hippocampal function. A new part of the theory introduced here is a quantitative analysis of how backprojections from the hippocampus to the neocortex could lead to the recall of recent memories. The theory is then compared with other theories of hippocampal function. First, what is computed by the hippocampus is considered. The hypothesis the authors advocate, on the basis of the effects of damage to the hippocampus and neuronal activity recorded in it, is that it is involved in the formation of new memories by acting as an intermediate-term buffer store for information about episodes, particularly for spatial, but probably also for some nonspatial, information. The authors analyze how the hippocampus could perform this function, by producing a computational theory of how it operates, based on neuroanatomical and neurophysiological information about the different neuronal systems con-tained within the hippocampus. Key hypotheses are that the CA3 pyramidal cells operate as a single autoassociation network to store new episodic information as it arrives via a number of specialized preprocessing stages from many association areas of the cerebral cortex, and that the dentate

The information represented in the primate hippocampus is being analysed by making recordings in monkeys actively walking in the laboratory. In a sample of 352 cells recorded in this situation, no "place" cells have so far been found. Instead, we have found a considerable population of "spatial view" cells tuned to respond when the monkey looks at small parts of the environment. We have been able to demonstrate (1) that these hippocampal neurons respond to a view of space "out there," not to the place where the monkey is; (2) that the responses depend on where the monkey is looking, by measuring eye position; (3) that the responses in some cases (e.g., CA1 but not CA3) still occur if the view details are obscured with curtains; (4) that the cells (in, e.g., CA1) retain part of their "space" tuning even in complete darkness, for several minutes; and (5) that the spatial representation is allocentric. The spatial representation is, thus, different from that in the rat hippocampus, in which place cells respond based on where the rat is located. The representation is also different from that described in the parietal cortex, where neurons respond in egocentric coordinates. This representation of space "out there" provided by primate spatial view cells would be an appropriate part of a memory system involved in memories of particular events or episodes, for example, of where in an environment an object was seen. Spatial view cells (in conjunction with whole body motion cells in the primate hippocampus, and head direction cells in the primate presubiculum) would also be useful as part of a spatial navigation system, for which they would provide a memory component. Hippocampus 1999;9:467--480. # 1999 Wiley-Liss, Inc.

assess dysfunction of the prefrontal cortex and basal ganglia. Previous brain imaging studies have focused on identifying activity related to the set-shifting requirement of the WCST. The present study used event-related functional magnetic resonance imaging (fMRI) to study the pattern of activation during four distinct stages in the performance of this task. Eleven subjects were scanned while performing the WCST and a control task involving matching two identical cards. The results demonstrated specific involvement of different prefrontal areas during different stages of task performance. The middorsolateral prefrontal cortex (area 9/46) increased activity while subjects received either positive or negative feedback, that is at the point when the current information must be related to earlier events stored in working memory. This is consistent The Wisconsin Card Sorting Task (WCST) has been used to

Introduction Remembering where a location is and how to get there (topographical memory) as well as what happened there (episodic memory) are cognitive operations thought to be dependent on the hippocampus and other medial temporal lobe structures (e.g. see Burgess et al., 1999). It has been suggested that the hippocampus stores a cognitive map of the spatial layout of an environment (O'Keefe and Nadel, 1978). It was further suggested that, in humans, it might additionally contain information about the spatiotemporal context of events. The ability to retrieve the context of an event is a defining characteristic of episodic memory, distinguishing it from simple familiarity-based recognition Oxford University Press 2001 patients were worse on tests of topographical memory, and the left temporal lobectomy (LTL) patients worse on tests of context-dependent episodic memory. Specifically, the RTL group was impaired on navigation, scene recognition and map drawing relative to control subje

INTRODUCTION Although our brains have developed exquisite mechanisms for recording speci# c experiences, it is not always advantageous for us to take the world too literally. A brain limited to storing an independent record of each experience would require a prodigious amount of storage and burden us with unnecessary details. Instead, we have evolved the ability to detect the commonalities among experiences and store them as abstract concepts, general principles and rules. This is an ef# cient way to deal with a complex world and allows the navigation of many different situations with a minimal amount of storage. It also allows us to deal with novelty. By extracting the essential elements from our experiences, we can generalize to future situations that share some elements but may, on the surface, appear very different. For example, consider the concept `camera'. We do not have to learn anew about every camera that we may encounter. Just knowing that the item is a camera communicates

We describe here hippocampal cells that respond during whole-body motion when a monkey is moved on a remote-controlled robot-mounted platform in a cue-controlled test chamber (2 x 2 x 2 m). Some of these cells responded to linear motion, and others to axial rotation. Some of these cells responded when the same motion occurred without a view of the visual field. Such cells appeared to be driven by vestibular inputs. Other cells required a view of the visual field for their response, and these cells appeared to be driv-en by the visual motion relative to the monkey of the test chamber. Further evidence that this was the case was that some of the cells responded to rotation and linear motion of the test chamber while the monkey remained stationary. Oth-er cells responded to combinations of whole-body motion and a view of the environment.

Although we often encounter circumstances with which we have no prior experience, we rapidly learn how to behave in these novel situations. Such adaptive behavior relies on abstract behavioral rules that are generalizable, rather than concrete rules mapping specific cues to specific responses. Although the frontal cortex is known to support concrete rule learning, less well understood are the neural mechanisms supporting the acquisition of abstract rules. Here, we use a reinforcement learning paradigm to demonstrate that more anterior regions along the rostro-caudal axis of frontal cortex support rule learning at higher levels of abstraction. Moreover, these results indicate that when humans confront new rule learning problems, this rostro-caudal division of labor supports the search for relationships between context and action at multiple levels of abstraction simultaneously.

A quantitative computational theory of the operation of the CA3 system as an attractor or autoassociation network is described. Based on the proposal that CA3–CA3 autoassociative networks are important for episodic or event memory in which space is a component (place in rodents and spatial view in primates), it has been shown behaviorally that the CA3 supports spatial rapid one-trial learning and learning of arbitrary associations and pattern completion where space is a component. Consistent with the theory, single neurons in the primate CA3 respond to combinations of spatial view and object, and spatial view and reward. Furthermore, single CA3 neurons reflect the recall of a place from an object in a one-trial object-place event memory task. CA3 neurons also reflect in their firing a memory of spatial view that is retained and updated by idiothetic information to implement path integration when the spatial view is obscured. Based on the computational proposal that the dentate gyrus produces sparse representations by competitive learning and via the mossy fiber pathway forces new representations on the CA3 during learning (encoding), it has been shown behaviorally that the dentate gyrus supports spatial pattern separation during learning, and that the mossy fiber system to CA3 connections are involved in learning but not in recall. The perforant path input to CA3 is quantitatively appropriate to provide the cue for recall in CA3. The concept that the CA1 recodes information from CA3 and sets up associatively learned back-projections to neocortex to allow subsequent retrieval of information to neocortex provides a quantitative account of the large number of

We studied the timecourse of neural activity in the primate (Macacca mulatta) prefrontal (PF) codex during an object delayedmatching -to-sample (DMS) task. To assess the effects of experience on this timecourse, we conducted the task using both novel and highly familiar objects. In addition, noise patterns containing no task-relevant information were used as samples on some trials. Comparison of average PF ensemble activity relative to baseline activity generated by objects and noise patterns revealed three distinct activity periods. (i) Sample onset elicited a transient sensory visual response. In this sensory period, novel objects elicited stronger average ensemble activity than both familiar objects and noise patterns. (ii) An intermediate period of elevated activity followed, which began before sample offset, and continued well into the delay period. In the intermediate period, activity was elevated for noise patterns and novel objects, but near baseline for familiar objects. (iii) Finally, after average ensemble activity reached baseline activity at the end of the intermediate period, a reactivation period occurred late in the delay. Experience had little effect during reactivation, where activity was elevated for both novel and familiar objects compared to noise patterns. We show that the ensemble average resembles the activity timecourse of many single prefrontal neurons. These results suggest that PF delay activity does not merely maintain recent sensory input, but is subject to more complex experiencedependent dynamics. This has implications for how delay activity is generated and maintained.

... (1988), this paper compares conscious and unconscious processes across waking, nonlucid, and lucid dreams. Sleep psychology can display gross functional dissociation between perceptual and cognitive consciousness. We utilize this observation to develop models of sleep experience and dream generation. These models accommodate Hunt’s (1989) “multiplicity of dreams”, as well as the intrinsic variation of perceptual and cognitive activity during dreaming. Lucid dreams are suggested to result from the presence of a skill-based mental set, the lucid dream context, which allows voluntary interaction with the spontaneous dream process. Our view of dreaming provides an explanation of the tendency of lucid dreams to either fade or revert to nonlucid dreams. Neurobiological considerations lead us to hypothesize that, in the sleeping brain, a reversal of information flow from medial temporal lobe mnemonic structures to thalamocortical perceptual circuits imparts parameterization to dream perceptual consciousness. A consequence of our thinking is that dreaming results in a “mental recombination” of cerebral information networks, which contributes to the ability of waking consciousness to generate novel and adaptive