In the mammalian hippocampus, the dentate gyrus (DG) is characterized by sparse and powerful unidirectional projections to CA3 pyramidal cells, the so-called mossy fibers. Mossy fiber synapses appear to duplicate, in terms of the information they convey, what CA3 cells already receive from entorhinal cortex layer II cells, which project both to the dentate gyrus and to CA3. Computational models of episodic memory have hypothesized that the function of the mossy fibers is to enforce a new, well separated pattern of activity onto CA3 cells, to represent a new memory, prevailing over the interference produced by the traces of older memories already stored on CA3 recurrent collateral connections. Can this hypothesis apply also to spatial representations, as described by recent neurophysiological recordings in rats? To address this issue quantitatively, we estimate the amount of information DG can impart on a new CA3 pattern of spatial activity, using both mathematical analysis and computer simulations of a simplified model. We confirm that, also in the spatial case, the observed sparse connectivity and level of activity are most appropriate for driving memory storage – and not to initiate retrieval. Surprisingly, the model also indicates that even when DG codes just for space, much of the information it passes on to CA3 acquires a non-spatial and episodic character, akin to that of a random number generator. It is suggested that further hippocampal processing is required to make full spatial use of DG inputs.

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Neural computation models have hypothesized that the dentate gyrus (DG) drives the storage in the CA3 network of new memories including, e.g., in rodents, spatial memories. Can recurrent CA3 connections self-organize, during storage, and form what have been called continuous attractors, or charts—so that they express spatial information later, when aside from a partial cue the information may not be available in the inputs? We use a simplified mathematical network model to contrast the properties of spatial representations self-organized through simulated Hebbian plasticity with those of charts pre-wired in the synaptic matrix, a control case closer to the ideal notion of continuous attractors. Both models form granular quasi-attractors, characterized by drift, which approach continuous ones only in the limit of an infinitely large network. The two models are comparable in terms of precision, but not of accuracy: with self-organized connections, the metric of space remains distorted, ill-adequate for accurate path integration, even when scaled up to the real hippocampus. While prolonged self-organization makes charts somewhat more informative about position in the environment, some positional information is surprisingly present also about environments never learned, borrowed, as it were, from unrelated charts. In contrast, context discrimination decreases with more learning, as different charts tend to collapse onto each other. These observations challenge the feasibility of the idealized CA3 continuous chart concept, and are consistent with a CA3 specialization for episodic memory rather than path integration.

Hippocampal place responses can be prospectively or retrospectively modulated by the animal's future or prior trajectory. Two main hypotheses explain this. The "multiple-map hypothesis" switches between different maps for different trajectories (rate remapping). In contrast, in the "buffer hypothesis," the hippocampus encodes an ongoing representation that includes the recent past and/or the impending future choice. This study examines the distribution of prospective and retrospective responses distributed along a common path in a continuous T-maze (providing all four combinations of provenance and destination) during a visual discrimination task. The multiple-map hypothesis predicts either uniform distributions or concerted shifts about a task-decision relevant point, whereas the buffer hypothesis predicts a time-limited overexpression around choice points (with retrospective responses after the central arm entry point and prospective responses nearer its exit). Here bilateral recordings in the dorsal CA1 region of the rat hippocampus show that retrospective responses were twice as prevalent as prospective responses. Furthermore, retrospective and prospective modulations have distinct spatial distributions, with retrospective primarily in the first two-thirds of the central arm and prospective restricted to the last third. To test for possible trial-by-trial remapping in relation to the two-thirds transition point, data from the first and second halves of the sessions were compared. Backward drift of path-modulated activity was significant only for retrospective, but not prospective, fields. Thus, these data are more consistent with the buffer hypothesis. Retrospective and prospective modulation would then participate in a single hippocampal representation of spatial and behavioral context.

Monkeys can learn the symbolic meaning of tokens, and exchange them to get a reward. Monkeys can also learn the symbolic value of a token by observing conspecifics but it is not clear if they can learn passively by observing other actors, e.g., humans. To answer this question, we tested two monkeys in a token exchange paradigm in three experiments. Monkeys learned token values through observation of human models exchanging them. We used, after a phase of object familiarization, different sets of tokens. One token of each set was rewarded with a bit of apple. Other tokens had zero value (neutral tokens). Each token was presented only in one set. During the observation phase, monkeys watched the human model exchange tokens and watched them consume rewards (vicarious rewards). In the test phase, the monkeys were asked to exchange one of the tokens for food reward. Sets of three tokens were used in the first experiment and sets of two tokens were used in the second and third experiments. The valuable token was presented with different probabilities in the observation phase during the first and second experiments in which the monkeys exchanged the valuable token more frequently than any of the neutral tokens. The third experiments examined the effect of unequal probabilities. Our results support the view that monkeys can learn from non-conspecific actors through vicarious reward, even a symbolic task like the token-exchange task.

How are neuronal representations of space organized in the hippocampus? The self-organization of such representations, thought to be driven in the CA3 network by the strong randomizing input from the Dentate Gyrus, appears to run against preserving the topology and even less the exact metric of physical space. We present a way to assess this issue quantitatively, and find that in a simple neural network model of CA3, the average topology is largely preserved, but the local metric is loose, retaining e.g., 10% of the optimal spatial resolution.

Place-selective activity in hippocampal neurons can be modulated by the trajectory that will be taken in the immediate future ("prospective coding"), information that could be useful in neural processes elaborating choices in route planning. To determine if and how hippocampal prospective neurons participate in decision making, we measured the time course of the evolution of prospective activity by recording place responses in rats performing a T-maze alternation task. After five or seven alternation trials, the routine was unpredictably interrupted by a photodetector-triggered visual cue as the rat crossed the middle of central arm, signaling it to suddenly change its intended choice. Comparison of the delays between light cue presentation and the onset of prospective activity for neurons with firing fields at various locations after the trigger point revealed a 420 ms processing delay. This surprisingly long delay indicates that prospective activity in the hippocampus appears much too late to generate planning or decision signals. This provides yet another example of a prominent brain activity that is unlikely to play a functional role in the cognitive function that it appears to represent (planning future trajectories). Nonetheless, the hippocampus may provide other contextual information to areas active at the earliest stages of selecting future paths, which would then return signals that help establish hippocampal prospective activity.

To solve novel problems, it is advantageous to abstract relevant information from past experience to transfer on related problems. To study whether macaque monkeys were able to transfer an abstract rule across cognitive domains, we trained two monkeys on a nonmatch-to-goal (NMTG) task. In the object version of the task (O-NMTG), the monkeys were required to choose between two object-like stimuli, which differed either only in shape or in shape and color. For each choice, they were required to switch from their previously chosen object-goal to a different one. After they reached a performance level of over 90% correct on the O-NMTG task, the monkeys were tested for rule transfer on a spatial version of the task (S-NMTG). To receive a reward, the monkeys had to switch from their previously chosen location to a different one. In both the O-NMTG and S-NMTG tasks, there were four potential choices, presented in pairs from trial-to-trial. We found that both monkeys transferred successfully the NMTG rule within the first testing session, showing effective transfer of the learned rule between two cognitive domains.