Construction and disruption of spatial memory networks during development

  1. Gregory L. Holmes6
  1. 1Department of Anatomy/Neurobiology, University of California-Irvine, Irvine, California 92697, USA
  2. 2Department of Pediatrics, University of California-Irvine, Irvine, California 92697, USA
  3. 3Department of Neurology, University of California-Irvine, Irvine, California 92697, USA
  4. 4Kavli Institute for Systems Neuroscience and Centre for Neural Computation, Norwegian University of Science and Technology, Trondheim 7491, Norway
  5. 5Biozentrum, Department of Cell Biology, University of Basel 4056, Switzerland
  6. 6Department of Neurological Sciences, University of Vermont College of Medicine, Burlington, Vermont 05401, USA
  1. Corresponding author: gregory.holmes{at}uvm.edu

Abstract

Spatial memory, the aspect of memory involving encoding and retrieval of information regarding one's environment and spatial orientation, is a complex biological function incorporating multiple neuronal networks. Hippocampus-dependent spatial memory is not innate and emerges during development in both humans and rodents. In children, nonhippocampal dependent egocentric (self-to-object) memory develops before hippocampal-dependent allocentric (object-to-object) memory. The onset of allocentric spatial memory abilities in children around 22 mo of age occurs at an age-equivalent time in rodents when spatially tuned grid and place cells arise from patterned activity propagating through the entorhinal–hippocampal circuit. Neuronal activity, often driven by specific sensory signals, is critical for the normal maturation of brain circuits This patterned activity fine-tunes synaptic connectivity of the network and drives the emergence of specific firing necessary for spatial memory. Whereas normal activity patterns are required for circuit maturation, aberrant neuronal activity during development can have major adverse consequences, disrupting the development of spatial memory. Seizures during infancy, involving massive bursts of synchronized network activity, result in impaired spatial memory when animals are tested as adolescents or adults. This impaired spatial memory is accompanied by alterations in spatial and temporal coding of place cells. The molecular mechanisms by which early-life seizures lead to disruptions at the cellular and network levels are now becoming better understood, and provide a target for intervention, potentially leading to improved cognitive outcome in individuals experiencing early-life seizures.

  • Received December 22, 2018.
  • Accepted April 2, 2019.

This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first 12 months after the full-issue publication date (see http://learnmem.cshlp.org/site/misc/terms.xhtml). After 12 months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

| Table of Contents