Considerations arising from a complementary learning systems perspective on hippocampus and neocortex

Abstract

We discuss a framework for the organization of learning systems in the mammalian brain , in which the hippocampus and related areas form a memory system complementary to learning mechanisms in neocortex and other areas. The hippocampal system stores new episodes and "replays" them to the neocortical system , interleaved with ongoing experience, allowing generalization as cortical memories form. The data to account for include: 1) neurophysiological findings concerning represen.tations in hippocampal areas, 2) behavioral evidence demonstrating a spatial role for hippocampus , 3) and effects of surgical and pharmacologi. cal manipulations on neuronal firing in hippocampal regions in behaving animals. We hypothesize that the hippocampal memory system consists of three major modules: 1) an invertible encoder subsystem supported by the pathways between neocortex and entorhinal cortex, which provides a stable, compressed, invertible encoding in entorhinal cortex (EC) of cortical activity patterns , 2) a memory separation, storage, and retrieval subsystem, supported by pathways between EC, dentate gyrus and area CA3, including the CA3 recurrent collaterals , which facilitates encoding and storage in CA3 of individual EC patterns, and retrieval of those CA3 encodings, in a manner that minimizes interference, and 3) a memory decoding subsystem, supported by the Shaffer collaterals from area CA 1 to area CA3 and the bi.directional pathways between EC and CA3, which provides the means by which a retrieved CA3 coding of an EC pattern can reinstate that pattern on Ec. This model has shown that 1) there is a trade-off between the need for information-preserving, structure. extracting encoding of cortical traces and the need for effective storage and recall of arbitrary traces, 2) long. term depression of synaptic strength in the pathways subject to long. term potentiation is crucial in preserving information, 3) area CA1 must be able to exploit correlations in EC patterns in the direct perforant path synapses.

Neurocognitive aging: prior memories hinder new hippocampal encoding

“…First, the DG is composed of roughly four times as many projection cells as the EC or CA3 [25]. This divergence and subsequent convergence of information has led to the idea that the DG might reduce the similarity of input patterns (pattern separation) [26,27]. Second, CA3 is unique within the hippocampus for containing recurrent connections: greater than 95% of input to each CA3 cell comes from CA3 collaterals.…”

“…Each hippocampal sub-region might make its own unique contribution to the impairment, as indicated in the model. Models of information processing describe two major functions that take place in the hippocampal network, pattern separation in the DG and pattern completion in CA3 [26,27]. For young rats, the hippocampal system is simulated as an attractor network, capable of maintaining a representation despite minor changes in external input from the EC.…”

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

“…We argue that this same representation is used in CA3, thus making possible fluent bidirectional exchange of information with the dentate. For the output of CA3 to influence cortical function, it must be turned back into the representation used by the cortex, and this appears to be one function of CA1 (Treves and Rolls, 1992;McClelland and Goddard, 1996). These ideas about "hippocampal" and "cortical" representations make it possible to account for a property of all the major excitatory connections.…”

A Dynamic Role of the Medial Temporal Lobe during Retrieval of Declarative Memory in Man

“…NI970276 consolidation (Bibbig et al, 1995;Brown, 1990;Eichenbaum, 1994;McClelland and Goddard, 1996;McClelland et al, 1995;Mesulam, 1990;Nadel, 1994;O'Reilly and McClelland, 1994;Shapiro and Olton, 1994;Squire, 1992;Squire and ZolaMorgan, 1991;Treves and Rolls, 1994). Distributed activity in the neocortex is thought to be the substrate for perception and short-term memory (Damasio and Damasio, 1994;Fuster, 1994;Mesulam, 1990;Singer and Gray, 1995).…”