Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.

  title={Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.},
  author={James L. McClelland and Bruce L. McNaughton and Randall C. O’Reilly},
  journal={Psychological review},
  volume={102 3},
Damage to the hippocampal system disrupts recent memory but leaves remote memory intact. The account presented here suggests that memories are first stored via synaptic changes in the hippocampal system, that these changes support reinstatement of recent memories in the neocortex, that neocortical synapses change a little on each reinstatement, and that remote memory is based on accumulated neocortical changes. Models that learn via changes to connections help explain this organization. These… 

Engrams and circuits crucial for systems consolidation of a memory

It is found that neocortical prefrontal memory engram cells, which are critical for remote contextual fear memory, were rapidly generated during initial learning through inputs from both the hippocampal–entorhinal cortex network and the basolateral amygdala.

Memory consolidation.

System consolidation is the process by which the hippocampus guides the reorganization of the information stored in the neocortex such that it eventually becomes independent of the hippocampus.

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

An account of how the hippocampus and neocortex can interact without any external input during sleep to drive useful new cortical learning and to protect old knowledge as new information is integrated is provided.

Shift from hippocampal to neocortical centered retrieval network with consolidation.

The results provide mechanistic support for a two-level process of the declarative memory system, involving initial representation of new associations in a network including the hippocampus and subsequent consolidation into a predominantly neocortical network.

Conjunctive representations in learning and memory: principles of cortical and hippocampal function.

This framework suggests that tasks involving rapid, incidental conjunctive learning are better tests of hippocampal function, and is implemented in a computational neural network model that can account for a wide range of data in animal learning.

Rapid and independent memory formation in the parietal cortex

Brain activity during virtual-reality navigation shows that contributions of hippocampus and parietal neocortex to memory are changing substantially already at the time a spatial memory representation is built, and shows that the posterior parietal cortex fulfills all criteria for a hippocampus-independent memory representation.

Complementary learning systems within the hippocampus: A neural network modeling approach to reconciling episodic memory with statistical learning

This work exposed a neural network model that instantiates known properties of hippocampal projections and subfields to sequences of items with temporal regularities and found that the monosynaptic pathway — the pathway connecting entorhinal cortex directly to region CA1 — was able to support statistical learning and memorization of individual episodes.

Neurocomputational model for learning, memory consolidation and schemas

It is proposed that the prefrontal cortex uses signals to modulate memory formation in the hippocampus during learning, which in turn influences consolidation during sleep replay, and provides theoretical framework to explain experimental findings and produce predictions for hippocampal-neocortical interactions during learning and systems consolidation.



Two functional components of the hippocampal memory system

It is proposed that neocortical association areas maintain shortterm memories for specific items and events prior to hippocampal processing as well as providing the final repositories of long-term memory.

Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia

How the theory can be applied to explain a wide range of impairments that have been observed when learning and memory tasks have been employed to assess the effect of hippocampal formation damage is illustrated.

The primate hippocampal formation: evidence for a time-limited role in memory storage.

Results show that the hippocampal formation is required for memory storage for only a limited period of time after learning, and as time passes, its role in memory diminishes, and a more permanent memory gradually develops independently of the hippocampus.

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  • Biology, Psychology
    Psychological review
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The role of the hippocampus is considered, which is needed temporarily to bind together distributed sites in neocortex that together represent a whole memory.

The hippocampal memory indexing theory.

It is asserted that the reactivation of the stored hippocampal memory index will serve to also reactivate the associated unique array of neocortical areas and thus will result in a memorial experience.

Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information

The hypothesis that memories are stored as a specific distribution of strengths in a population of modifiable synapses was examined, and the bilateral induction of long-term enhancement in synapses of the main afferent fiber system to the hippocampal formation in rats supported the hypothesis that, during the formation of “cognitive maps,” spatial information must be temporarily stored at modifiablesynapses at the input stage to the hippocampus.

Computational analysis of the role of the hippocampus in memory

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 by producing a computational theory of how it operates, based on neuroanatomical and neurophysiological information about the different neuronal systems contained within the hippocampus.

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The modified theory explains why damage to the hippocampal formation only impairs learning on a subset of nonlinear discrimination problems and makes novel predictions about performance on nonlineardiscrimination problems and place learning.

Hippocampal synaptic enhancement and information storage within a distributed memory system