The neurotransmitter dopamine (DA) plays an important role in learning by enhancing the saliency of behaviorally relevant stimuli. How this stimulus selection is achieved on the cellular level, however, is not known. Here, in recordings from hippocampal slices, we show that DA acts specifically at the direct cortical input to hippocampal area CA1 (the temporoammonic (TA) pathway) to filter the excitatory drive onto pyramidal neurons based on the input frequency. During low-frequency patterns of stimulation, DA depressed excitatory TA inputs to both CA1 pyramidal neurons and local inhibitory GABAergic interneurons via presynaptic inhibition. In contrast, during high-frequency patterns of stimulation, DA potently facilitated the TA excitatory drive onto CA1 pyramidal neurons, owing to diminished feedforward inhibition. Analysis of DA's effects over a broad range of stimulus frequencies indicates that it acts as a high-pass filter, augmenting the response to high-frequency inputs while diminishing the impact of low-frequency inputs. These modulatory effects of DA exert a profound influence on activity-dependent forms of synaptic plasticity at both TA-CA1 and Schaffer-collateral (SC)-CA1 synapses. Taken together, our data demonstrate that DA acts as a gate on the direct cortical input to the hippocampus, modulating information flow and synaptic plasticity in a frequency-dependent manner.
Keywords: hippocampus, area CA1, dopamine, temporoammonic pathway, frequency-dependent filter, LTP, LTD
Citation: Hiroshi T. Ito and Erin M. Schuman (2007). Frequency-dependent gating of synaptic transmission and plasticity by dopamine. Front. Neural Circuits 1:1. doi: 10.3389/neuro.04/001.2007
Received: 25 June 2007;
Paper pending published: 17 September 2007;
Accepted: 15 October 2007; Published online: 2 November 2007.
Edited by:Rafael Yuste, Columbia University, New York City, USA
Reviewed by:Gabor Tamas, University of Szeged, Hungary
Copyright: © 2007 Ito, Schuman. This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.
*Correspondence: Erin M. Schuman, Division of Biology, California Institute of Technology and Howard Hughes Medical Institute, 1200 E. California Blvd, Pasadena, CA 91125, USA. e-mail: firstname.lastname@example.org