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Cerebral Cortex Advance Access published online on June 11, 2008

Cerebral Cortex, doi:10.1093/cercor/bhn101
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© 2008 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/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Synapsin- and Actin-Dependent Frequency Enhancement in Mouse Hippocampal Mossy Fiber Synapses

Simen G. Owe1,2, Vidar Jensen3, Emma Evergren4, Arnaud Ruiz5, Oleg Shupliakov4, Dimitri M. Kullmann5, Jon Storm-Mathisen1,2, S. Ivar Walaas3, Øivind Hvalby3 and Linda H. Bergersen1,2

1 Department of Anatomy, Institute of Basic Medical Sciences, 2 Centre for Molecular Biology and Neuroscience, 3 Molecular Neurobiology Research Group, Institute of Basic Medical Sciences, University of Oslo, PO Box 1105, Blindern, N-0317 Oslo, Norway, 4 Department of Neuroscience, Linné Centre for Developmental Biology and Regenerative Medicine, Karolinska Institutet, 17177 Stockholm, Sweden, 5 Institute of Neurology, University College London, London WC1N 3BG, UK

Address correspondence to email: l.h.bergersen{at}medisin.uio.no.

The synapsin proteins have different roles in excitatory and inhibitory synaptic terminals. We demonstrate a differential role between types of excitatory terminals. Structural and functional aspects of the hippocampal mossy fiber (MF) synapses were studied in wild-type (WT) mice and in synapsin double-knockout mice (DKO). A severe reduction in the number of synaptic vesicles situated more than 100 nm away from the presynaptic membrane active zone was found in the synapsin DKO animals. The ultrastructural level gave concomitant reduction in F-actin immunoreactivity observed at the periactive endocytic zone of the MF terminals. Frequency facilitation was normal in synapsin DKO mice at low firing rates (~0.1 Hz) but was impaired at firing rates within the physiological range (~2 Hz). Synapses made by associational/commissural fibers showed comparatively small frequency facilitation at the same frequencies. Synapsin-dependent facilitation in MF synapses of WT mice was attenuated by blocking F-actin polymerization with cytochalasin B in hippocampal slices. Synapsin III, selectively seen in MF synapses, is enriched specifically in the area adjacent to the synaptic cleft. This may underlie the ability of synapsin III to promote synaptic depression, contributing to the reduced frequency facilitation observed in the absence of synapsins I and II.

Key Words: actin filaments • frequency facilitation • hippocampal synapses • immunoelectron microscopy • presynaptic plasticity


Simen G. Owe and Vidar Jensen contributed equally to this work


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