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J Neurophysiol 102: 2763-2770, 2009. First published September 2, 2009; doi:10.1152/jn.00347.2009
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00347.2009v1
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RESEARCH-ARTICLE

Intrinsic Neuronal Excitability Is Reversibly Altered by a Single Experience in Fear Conditioning

Bridget M. McKay*, Elizabeth A. Matthews*, Fernando A. Oliveira and John F. Disterhoft

Department of Physiology, Northwestern University, Chicago, Illinois

Submitted 17 April 2009; accepted in final form 31 August 2009

ABSTRACT

Learning is known to cause alterations in intrinsic cellular excitability but, to date, these changes have been seen only after multiple training trials. A powerful learning task that can be quickly acquired and extinguished with a single trial is fear conditioning. Rats were trained and extinguished on a hippocampus-dependent form of fear conditioning to determine whether learning-related changes in intrinsic excitability could be observed after a few training trials and a single extinction trial. Following fear training, hippocampal slices were made and intrinsic excitability was assayed via whole cell recordings from CA1 neurons. Alterations in intrinsic excitability, assayed by the postburst afterhyperpolarization and firing frequency accommodation, were observed after only three trials of contextual or trace-cued fear conditioning. Animals that had been trained in contextual and trace-cued fear were then extinguished. Context fear-conditioned animals extinguished in a single trial and the changes in intrinsic excitability were reversed. Trace-cue conditioned animals only partially extinguished in a single trial and reductions in excitability remained. Thus a single learning experience is sufficient to alter intrinsic excitability. This dramatically extends observations of learning-specific changes in intrinsic neuronal excitability previously observed in paradigms requiring many training trials, suggesting the excitability changes have a basic role in acquiring new information.


Address for reprint requests and other correspondence: B. M. McKay, 303 E. Chicago Ave., Ward 7-140, Chicago, IL 60611 (E-mail: BridgetMcKay2010{at}u.northwestern.edu).







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