Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema

J Neurosci. 2013 Jun 19;33(25):10243-56. doi: 10.1523/JNEUROSCI.0879-13.2013.

Abstract

According to schema theory as proposed by Piaget and Bartlett, learning involves the assimilation of new memories into networks of preexisting knowledge, as well as alteration of the original networks to accommodate the new information. Recent evidence has shown that rats form a schema of goal locations and that the hippocampus plays an essential role in adding new memories to the spatial schema. Here we examined the nature of hippocampal contributions to schema updating by monitoring firing patterns of multiple CA1 neurons as rats learned new goal locations in an environment in which there already were multiple goals. Before new learning, many neurons that fired on arrival at one goal location also fired at other goals, whereas ensemble activity patterns also distinguished different goal events, thus constituting a neural representation that linked distinct goals within a spatial schema. During new learning, some neurons began to fire as animals approached the new goals. These were primarily the same neurons that fired at original goals, the activity patterns at new goals were similar to those associated with the original goals, and new learning also produced changes in the preexisting goal-related firing patterns. After learning, activity patterns associated with the new and original goals gradually diverged, such that initial generalization was followed by a prolonged period in which new memories became distinguished within the ensemble representation. These findings support the view that consolidation involves assimilation of new memories into preexisting neural networks that accommodate relationships among new and existing memories.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / physiology
  • Algorithms
  • Animals
  • Bayes Theorem
  • Behavior, Animal / physiology
  • CA1 Region, Hippocampal / cytology
  • CA1 Region, Hippocampal / physiology
  • Conditioning, Operant / physiology
  • Cues
  • Electrodes, Implanted
  • Electrophysiological Phenomena
  • Goals
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Learning / physiology*
  • Male
  • Neurons / physiology*
  • Photic Stimulation
  • Principal Component Analysis
  • Rats
  • Rats, Long-Evans
  • Reward
  • Running / physiology