Structural synaptic plasticity has high memory capacity and can explain graded amnesia, catastrophic forgetting, and the spacing effect

PLoS One. 2014 May 23;9(5):e96485. doi: 10.1371/journal.pone.0096485. eCollection 2014.

Abstract

Although already William James and, more explicitly, Donald Hebb's theory of cell assemblies have suggested that activity-dependent rewiring of neuronal networks is the substrate of learning and memory, over the last six decades most theoretical work on memory has focused on plasticity of existing synapses in prewired networks. Research in the last decade has emphasized that structural modification of synaptic connectivity is common in the adult brain and tightly correlated with learning and memory. Here we present a parsimonious computational model for learning by structural plasticity. The basic modeling units are "potential synapses" defined as locations in the network where synapses can potentially grow to connect two neurons. This model generalizes well-known previous models for associative learning based on weight plasticity. Therefore, existing theory can be applied to analyze how many memories and how much information structural plasticity can store in a synapse. Surprisingly, we find that structural plasticity largely outperforms weight plasticity and can achieve a much higher storage capacity per synapse. The effect of structural plasticity on the structure of sparsely connected networks is quite intuitive: Structural plasticity increases the "effectual network connectivity", that is, the network wiring that specifically supports storage and recall of the memories. Further, this model of structural plasticity produces gradients of effectual connectivity in the course of learning, thereby explaining various cognitive phenomena including graded amnesia, catastrophic forgetting, and the spacing effect.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Amnesia / pathology
  • Amnesia / physiopathology*
  • Brain / pathology
  • Brain / physiopathology
  • Cognition / physiology
  • Humans
  • Memory / physiology*
  • Models, Neurological*
  • Nerve Net / pathology
  • Nerve Net / physiopathology
  • Neuronal Plasticity*
  • Neurons / cytology
  • Neurons / pathology
  • Synapses / physiology

Grants and funding

FTS received support from the National Science Foundation through the grants NSF-0855272 and NSF-1219212. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.