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The Journal of Neuroscience, October 7, 2009, 29(40):12597-12605; doi:10.1523/JNEUROSCI.2407-09.2009

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Behavioral/Systems/Cognitive
Alteration of Theta Timescale Dynamics of Hippocampal Place Cells by a Cannabinoid Is Associated with Memory Impairment

David Robbe^1,2 and György Buzsáki¹

¹Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102, and ²Institut d'Investigacions Biomediques August Pi i Sunyer, 08036 Barcelona, Spain

Correspondence should be addressed to either of the following: David Robbe, Institut d'Investigacions Biomediques August Pi i Sunyer, Carrer Corsega, 176, 08036 Barcelona, Spain, Email: davrobbe{at}clinic.ub.es; or György Buzsáki, Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, Email: buzsaki{at}axon.rutgers.edu

The integrity of the hippocampus is critical for both spatial navigation and episodic memory, but how its neuronal firing patterns underlie those functions is not well understood. In particular, the modality by which hippocampal place cells contribute to spatial memory is debated. We found that administration of the cannabinoid receptor agonist CP55940 (2-[(1S,2R,5S)-5-hydroxy-2-(3-hydroxypropyl)cyclohexyl]-5-(2-methyloctan-2-yl)phenol) induced a profound and reversible behavioral deficit in the hippocampus-dependent delayed spatial alternation task. On the one hand, despite severe memory impairment, the location-dependent firing of CA1 hippocampal place cells remained mostly intact. On the other hand, both spike-timing coordination between place cells at the theta timescale and theta phase precession of spikes were reversibly reduced. These results raise the possibility that cannabinoids impair memory primarily by altering short-term temporal dynamics of hippocampal neurons. We hypothesize that precise temporal coordination of hippocampal neurons is necessary for guiding behavior in spatial memory tasks.

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Received May 22, 2009; revised July 14, 2009; accepted Aug. 24, 2009.

Correspondence should be addressed to either of the following: David Robbe, Institut d'Investigacions Biomediques August Pi i Sunyer, Carrer Corsega, 176, 08036 Barcelona, Spain, Email: davrobbe{at}clinic.ub.es; or György Buzsáki, Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102, Email: buzsaki{at}axon.rutgers.edu

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