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The Journal of Neuroscience, April 30, 2008, 28(18):4592-4603; doi:10.1523/JNEUROSCI.5354-07.2008

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Behavioral/Systems/Cognitive
Dendritic Design Implements Algorithm for Synaptic Extraction of Sensory Information

Hiroto Ogawa,¹ Graham I. Cummins,² Gwen A. Jacobs,² and Kotaro Oka³

¹Department of Biology, Faculty of Medicine, Saitama Medical University, Saitama 350-0496, Japan, ²Center for Computational Biology, Montana State University, Bozeman, Montana 59717, and ³Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Yokohama 223-8522, Japan

Correspondence should be addressed to Dr. Hiroto Ogawa, Department of Biology, Faculty of Medicine, Saitama Medical University, 981 Kawakado, Moroyama, Iruma-gun, Saitama 350-0496, Japan. Email: hogawa{at}saitama-med.ac.jp

While sensory information is encoded by firing patterns of individual sensory neurons, it is also represented by spatiotemporal patterns of activity in populations of the neurons. Postsynaptic interneurons decode the population response and extract specific sensory information. This extraction of information represented by presynaptic activities is a process critical to defining the input–output function of postsynaptic neuron. To understand the "algorithm" for the extraction, we examined directional sensitivities of presynaptic and postsynaptic Ca²⁺ responses in dendrites of two types of wind-sensitive interneurons (INs) with different dendritic geometries in the cricket cercal sensory system. In IN 10-3, whose dendrites arborize with various electrotonic distances to the spike-initiating zone (SIZ), the directional sensitivity of dendritic Ca²⁺ responses corresponded to those indicated by Ca²⁺ signals in presynaptic afferents arborizing on that dendrite. The directional tuning properties of individual dendrites varied from each other, and the directional sensitivity of the nearest dendrite to the SIZ dominates the tuning properties of the spiking response. In IN 10-2 with dendrites isometric to the SIZ, directional tuning properties of different dendrites were similar to each other, and each response property could be explained by the directional profile of the spatial overlap between that dendrite and Ca²⁺-elevated presynaptic terminals. For IN 10-2, the directional sensitivities extracted by the different dendritic-branches would contribute equally to the overall tuning. It is possible that the differences in the distribution of synaptic weights because of the dendritic geometry are related to the algorithm for extraction of sensory information in the postsynaptic interneurons.

Key words: decoding; Ca²⁺-sensitive dye; optical recording; dendrites; insect; directional sensitivity

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Received Aug. 13, 2007; revised March 24, 2008; accepted March 24, 2008.

Correspondence should be addressed to Dr. Hiroto Ogawa, Department of Biology, Faculty of Medicine, Saitama Medical University, 981 Kawakado, Moroyama, Iruma-gun, Saitama 350-0496, Japan. Email: hogawa{at}saitama-med.ac.jp

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