Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off

Abstract

The hippocampus and related structures are thought to be capable of 1) representing cortical activity in a way that minimizes overlap of the representations assigned to different cortical patterns (pattern separation); and 2) modifying synaptic connections so that these representations can later be reinstated from partial or noisy versions of the cortical activity pattern that was present at the time of storage (pattern completion). We point out that there is a trade-off between pattern separation and completion and propose that the unique anatomical and physiological properties of the hippocampus might serve to minimize this trade-off. We use analytical methods to determine quantitative estimates of both separation and completion for specified parameterized models of the hippocampus. These estimates are then used to evaluate the role of various properties and of the hippocampus, such as the activity levels seen in different hippocampal regions, synaptic potentiation and depression, the multi-layer connectivity of the system, and the relatively focused and strong mossy fiber projections. This analysis is focused on the feedforward pathways from the entorhinal cortex (EC) to the dentate gyrus (DG) and region CA3. Among our results are the following: 1) Hebbian synaptic modification (LTP) facilitates completion but reduces separation, unless the strengths of synapses from inactive presynaptic units to active postsynaptic units are reduced (LTD). 2) Multiple layers, as in EC to DG to CA3, allow the compounding of pattern separation, but not pattern completion. 3) The variance of the input signal carried by the mossy fibers is important for separation, not the raw strength, which may explain why the mossy fiber inputs are few and relatively strong, rather than many and relatively weak like the other hippocampal pathways. 4) The EC projects to CA3 both directly and indirectly via the DG, which suggests that the two-stage pathway may dominate during pattern separation and the one-stage pathway may dominate during completion; methods the hippocampus may use to enhance this effect are discussed.

Self-organization in the olfactory system: one shot odor recognition in insects

“…As the MB is not the only olfactory pathway and has been shown to not be essential for basic odor perceptions by ablation experiments [16,7] this mode of failure should be interpreted as a failure to remember all classes rather than as a failure to perceive input odors. In contrast to an n-winner-take-all representation [33], the self-organized representation of odors in our system is solely determined by the learning rule, connectivity and type of activity in the system. Other, e.g., non-disjoint, representations were not observed even when changing the learning rule parameters or the maximal conductances of iKC-eKC synapses.…”

Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

“…Additionally or alternatively, the mossy fiber pathway could contribute to pattern separation [66,78]. The sparse connectivity between dentate gyrus granule cells and CA3 pyramidal neurons [4] and the differential dynamics of mossy fiber synapses on pyramidal neurons, which facilitate markedly, and those on interneurons, which facilitate less or even depress [80], may implement a "winner takes all" mechanism in which only the most active granule cells relay excitation to the CA3 network.…”

The hippocampal debate: are we asking the right questions?

“…Distinctions can be drawn between acti6e memory (in which a representation of the stimulus is held in neural activity) [55,64,252], filtering mechanisms (in which individual neurons respond differently to novel and to familiar objects [114,115], probably an implementation of perceptual priming [240]), and content-addressable memories (memory stored in interneuronal connections, presumably through LTPlike mechanisms) [75,83,110,156,171,184]. Each of these processes have advantages and disadvantages.…”

“…Filtering mechanisms seem to occur in sensory systems (such as inferotemporal cortex [114,115]). Content-addressable memory systems are usually attributed to the 'hippocampal formation' [33,156,184]. The question remains, however, whether these mechanisms are truly hippocampal or whether they preferentially involve the nearby cortical structures.…”