Memory consolidation and the medial temporal lobe: a simple network model.

Abstract

Some forms of memory have been shown to depend on a system of medial temporal lobe stuctlres that includes the hippocampus and the adjacent cortical areas (entorhinal, perirhinal, and parahippocampal cortex). The role of this system is only temporary, however, as indicated by the fact that, after damage to the medial temporal lobe, recent memories are impaired but very remote memories are Intact. Here we review the evidence that the medial temporal lobe memory system is involved in a process of consolidation: memories are initially dependent on this system but gradually become established in other areas of the brain. We then review some of the ideas that have been proposed about the phenomenon of consolidation and suggest a synthesis of these views. Finally, we describe a simple neural network model that captures some key features of consolidation.The importance of the medial temporal lobe (MTL) for human memory was established in the 1950s, when surgical removal of this region was found to produce a profound and selective memory impairment (1). Subsequent work, using a model of human amnesia in the monkey (2, 3), identified the anatomical components of this brain system-i.e., the hippocampus (together with the dentate gyrus and subiculum) and the adjacent, anatomically related entorhinal, perirhinal, and parahippocampal cortices. Continuing studies in humans, monkeys, and rodents have illuminated how this system contributes to memory functions (for review, see ref. 4).One important finding is that the MTL (and related structures in the diencephalic midline) is involved in a limited domain oflearning and memory. These structures support the capacity for conscious recollections of facts and events (i.e., declarative memory) but are not necessary for various nonconscious (nondeclarative) forms of memory that are expressed through performance, including skills and habits, simple forms ofconditioning, and the phenomenon ofpriming (5-7). Retrograde Amnesia and Memory ConsolidationA second important finding (and the focus of this article) is that the role of the MTL is only temporary. This conclusion is based on the fact that damage to the MTL produces temporally graded retrograde amnesia. Memory for events that occurred a short time before the damage is impaired, but memory for remote events (events that occurred a long time before the damage) is spared. This phenomenon was recognized more than a century ago as central to understanding memory and the brain (8). Since that time, temporally graded retrograde amnesia has been observed repeatedly in rodents and humans using a variety of memory tasks and disruptive treatments (9)(10)(11) Thus, as time passes after learning, there must be gradual reorganization (consolidation) of memory storage, whereby memories that are initially dependent on the MTL eventually do not require this system. A more permanent memory that is independent ofthe MTL develops gradually, presumably in neocortex (2,6,21).An alternative view is that consolidation occurs gradually but independ...

The hippocampal debate: are we asking the right questions?

“…A key question becomes whether the spatial and non-spatial correlations are equivalent or not. Memory theories suggest that they are equivalent [4,33,46,246], while spatial theories suggest that nonspatial variables are second-order effects [177,196,225], or even deny their existence [147]. What I am proposing here is that spatial and non-spatial correlations are both important, that they follow from similar processes, but that they show very different properties.…”

“…A good example of this is in one of the original studies used in the meta-analysis by Zola et al [4]. In this study, monkeys were given radio-frequency hippocampal lesions, and tested at the delays listed above.…”

“…And animal studies attempting to study recent declarative memory are inconsistent in their conclusions as to whether the hippocampus is involved in declarative memory or not [4,26,27 [4,26,27,32,45,70,113,119,133,135,137,253,257,258]. As with the water maze for spatial cognition, the DNMS task is a complex task that can be solved in a number of ways.…”

“…In this study, monkeys were given radio-frequency hippocampal lesions, and tested at the delays listed above. The monkeys only showed impairments at 10 and at 40 min delays [4]. However, the monkeys were returned to their home cages for the 10 and 40 min delays.…”

“…If the accumbens plays a role in action selection [68,124,163], and the entorhinal cortex plays a role in memory formation [28,138,214,218,244], then it is possible that the same internal information is redistributed in different ways across the two pathways. Navigation models extending to anatomical structures beyond hippocampus have tended to include models of accumbens as the 'next stage downstream' [19,22,53,177], while memory models have tended to emphasize the entorhinal-hippocampusentorhinal loop [4,24,33].…”