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Cerebral Cortex Advance Access published online on November 10, 2009
Cerebral Cortex, doi:10.1093/cercor/bhp184
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Frequency Facilitation at Mossy Fiber–CA3 Synapses of Freely Behaving Rats Contributes to the Induction of Persistent LTD via an Adenosine-A1 Receptor-Regulated Mechanism

Hardy Hagena1,2 and Denise Manahan-Vaughan1,2

1 Department of Experimental Neurophysiology, Medical Faculty, Ruhr University Bochum, 44780 Bochum, Germany, 2 International Graduate School for Neuroscience, Ruhr University Bochum, 44780 Bochum, Germany

Address correspondence to Denise Manahan-Vaughan, PhD, Department of Experimental Neurophysiology, Medical Faculty, Ruhr University Bochum, MABF 01/551, Universitaetsstrasse, 150, 44780 Bochum, Germany. Email: dmv-igsn{at}rub.de.

Frequency facilitation (FF), comprising a rapid and multiple-fold increase in the magnitude of evoked field potentials, is elicited by low-frequency stimulation (LFS) at mossy fiber–CA3 synapses. Here, we show that in freely behaving rats, FF reliably occurs in response to 1 and 2Hz but not in response to 0.25-, 0.3-, or 0.5-Hz LFS. Strikingly, prolonged (~600 s) FF was tightly correlated to the induction of long-term depression (LTD) in freely moving animals. Although LFS at 2 Hz elicited unstable FF and unstable LTD, application of LFS at 1 Hz elicited pronounced FF, as well as robust LTD that persisted for over 24 h. This correlation of prolonged FF with LTD was absent at stimulation frequencies that did not induce FF. The adenosine-A1 receptor appears to participate in these effects: Application of adenosine-A1, but not adenosine-A3, receptor antagonists enhanced mossy fiber synaptic transmission and occluded FF. Furthermore, adenosine-A1 receptor antagonism resulted in more stable FF at 1 or 2 Hz and elicited more potent LTD. These data support the fact that FF contributes to the enablement of long-term information storage at mossy fiber–CA3 synapses and that the adenosine-A1 receptor may regulate the thresholds for this process.

Key Words: CA3 • frequency facilitation • hipocampus • in vivo • long-term depression • mossy fiber • synaptic plasticity

Received for publication April 28, 2009. Revision received July 9, 2009. Accepted for publication July 23, 2009.


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