Distinct contributions of hippocampal NMDA and AMPA receptors to encoding and retrieval of one-trial place memory

J Neurosci. 2005 Jun 22;25(25):5845-56. doi: 10.1523/JNEUROSCI.0698-05.2005.

Abstract

Allocentric place memory may serve to specify the context of events stored in human episodic memory. Recently, our laboratory demonstrated that, analogous to event-place associations in episodic memory, rats could associate, within one trial, a specific food flavor with an allocentrically defined place in an open arena. Encoding, but not retrieval, of such flavor-place associations required hippocampal NMDA receptors; retrieval depended on hippocampal AMPA receptors. This might have partly reflected the contributions of these receptors to encoding and retrieval of one-trial place, rather than flavor-place, memory. Therefore, the present study developed a food-reinforced arena paradigm to study encoding and retrieval of one-trial allocentric place memory in rats; memory relied on visuospatial information and declined with increasing retention delay, still being significant after 6 h, the longest delay tested (experiments 1 and 2). Hippocampal infusion of the NMDA receptor antagonist d-AP-5 blocked encoding without affecting retrieval; hippocampal infusion of the AMPA receptor antagonist CNQX impaired retrieval (experiment 3). Finally, we confirmed that the d-AP-5 infusions selectively blocked induction of long-term potentiation, a form of synaptic plasticity, whereas CNQX impaired fast excitatory transmission, at perforant-path dentate gyrus synapses in the dorsal hippocampus in vivo (experiment 4). Our results support that encoding, but not retrieval, of one-trial allocentric place memory requires the NMDA receptor-dependent induction of hippocampal synaptic plasticity, whereas retrieval depends on AMPA receptor-mediated fast excitatory hippocampal transmission. The contributions of hippocampal NMDA and AMPA receptors to one-trial allocentric place memory may be central to episodic memory and related episodic-like forms of memory in rats.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Excitatory Amino Acid Antagonists / pharmacology
  • Habituation, Psychophysiologic
  • Hippocampus / physiology*
  • Male
  • Memory / physiology*
  • Models, Animal
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology
  • Rats
  • Rats, Inbred Strains
  • Receptors, AMPA / physiology*
  • Receptors, N-Methyl-D-Aspartate / physiology*
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology

Substances

  • Excitatory Amino Acid Antagonists
  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-Amino-5-phosphonovalerate