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The Journal of Neuroscience, June 22, 2005, 25(25):5845-5856; doi:10.1523/JNEUROSCI.0698-05.2005

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Behavioral/Systems/Cognitive
Distinct Contributions of Hippocampal NMDA and AMPA Receptors to Encoding and Retrieval of One-Trial Place Memory

Tobias Bast, Bruno M. da Silva, and Richard G. M. Morris

Laboratory for Cognitive Neuroscience, Division of Neuroscience, University of Edinburgh, Edinburgh EH8 9JZ, United Kingdom

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.

Key words: allocentric spatial learning; hippocampus; synaptic plasticity; NMDA; microinfusions; episodic-like memory

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Received Feb 21, 2005; revised April 14, 2005; accepted May 4, 2005.

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