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The Journal of Neuroscience, October 28, 2009, 29(43):13649-13661; doi:10.1523/JNEUROSCI.2672-09.2009

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Cellular/Molecular
Dendritic Compartment and Neuronal Output Mode Determine Pathway-Specific Long-Term Potentiation in the Piriform Cortex

Friedrich W. Johenning,¹ Prateep S. Beed,¹ Thorsten Trimbuch,² Michael H. K. Bendels,^1,3 Jochen Winterer,¹ and Dietmar Schmitz^1,4

¹Neuroscience Research Center, ²Institute for Cell Biology and Neurobiology, Center for Anatomy, and ³Neurophysics Group, Department of Neurology, Charité-Universitätsmedizin Berlin, 10117 Berlin, Germany, and ⁴Bernstein Center for Computational Neuroscience Berlin, 10115 Berlin, Germany

Correspondence should be addressed to either Dietmar Schmitz or Friedrich W. Johenning, Neurowissenschaftliches Forschungszentrum, Charité-Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, Germany. Email: dietmar.schmitz{at}charite.de or Email: friedrich.johenning{at}charite.de

The apical dendrite of layer 2/3 pyramidal cells in the piriform cortex receives two spatially distinct inputs: one projecting onto the distal apical dendrite in sensory layer 1a, the other targeting the proximal apical dendrite in layer 1b. We observe an expression gradient of A-type K⁺ channels that weakens the backpropagating action potential-mediated depolarization in layer 1a compared with layer 1b. We find that the pairing of presynaptic and postsynaptic firing leads to significantly smaller Ca²⁺ signals in the distal dendritic spines in layer 1a compared with the proximal spines in layer 1b. The consequence is a selective failure to induce long-term potentiation (LTP) in layer 1a, which can be rescued by pharmacological enhancement of action potential backpropagation. In contrast, LTP induction by pairing presynaptic and postsynaptic firing is possible in layer 1b but requires bursting of the postsynaptic cell. This output mode strongly depends on the balance of excitation and inhibition in the piriform cortex. We show, on the single-spine level, how the plasticity of functionally distinct synapses is gated by the intrinsic electrical properties of piriform cortex layer 2 pyramidal cell dendrites and the cellular output mode.

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Received June 8, 2009; revised July 24, 2009; accepted Aug. 5, 2009.

Correspondence should be addressed to either Dietmar Schmitz or Friedrich W. Johenning, Neurowissenschaftliches Forschungszentrum, Charité-Universitätsmedizin Berlin, Charitéplatz 1, 10117 Berlin, Germany. Email: dietmar.schmitz{at}charite.de or Email: friedrich.johenning{at}charite.de

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