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Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure reliable transmission
Authors:Bagnall Martha W  Hull Court  Bushong Eric A  Ellisman Mark H  Scanziani Massimo
Institution:1 Center for Neural Circuits and Behavior, University of California, San Diego, La Jolla, CA 92093, USA
2 Neurobiology Section, Division of Biology, University of California, San Diego, La Jolla, CA 92093, USA
3 National Center for Microscopy and Imaging Research, Center for Research in Biological Systems, Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093, USA
4 Howard Hughes Medical Institute, La Jolla, CA 92093, USA
Abstract:Thalamic afferents supply the cortex with sensory information by contacting both excitatory neurons and inhibitory interneurons. Interestingly, thalamic contacts with interneurons constitute such a powerful synapse that even one afferent can fire interneurons, thereby driving feedforward inhibition. However, the spatial representation of this potent synapse on interneuron dendrites is poorly understood. Using Ca imaging and electron microscopy we show that an individual thalamic afferent forms multiple contacts with the interneuronal proximal dendritic arbor, preferentially near branch points. More contacts are correlated with larger amplitude synaptic responses. Each contact, consisting of a single bouton, can release up to seven vesicles simultaneously, resulting in graded and reliable Ca transients. Computational modeling indicates that the release of multiple vesicles at each contact minimally reduces the efficiency of the thalamic afferent in exciting the interneuron. This strategy preserves the spatial representation of thalamocortical inputs across the dendritic arbor over a wide range of release conditions.
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