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Multiple-site optical recording for characterization of functional synaptic organization of the optic tectum of rainbow trout

Authors

  • Masae Kinoshita,

    1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060–0810, Japan
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  • Risa Ueda,

    1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060–0810, Japan
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  • Satoshi Kojima,

    1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060–0810, Japan
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    • *

      Present address: Keck Foundation Center for Integrative Neuroscience, Department of Physiology and Psychiatry, University of California, San Francisco, San Francisco, CA 94143, USA

  • Katsushige Sato,

    1. Department of Physiology, Tokyo Medical and Dental University, Graduate School and Faculty of Medicine, Tokyo 113–8519, Japan
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  • Masahiko Watanabe,

    1. Department of Anatomy, Hokkaido University School of Medicine, Sapporo 060–8638, Japan
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  • Akihisa Urano,

    1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060–0810, Japan
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  • Etsuro Ito

    1. Division of Biological Sciences, Graduate School of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060–0810, Japan
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: Dr Etsuro Ito, as above.
E-mail: eito@sci.hokudai.ac.jp

Abstract

To map the functional synaptic organization over a wide area in the optic tectum, we directly monitored two-dimensional propagation of postsynaptic depolarization evoked by firing of retinotectal afferents in optic tectum slices prepared from rainbow trout (Oncorhynchus mykiss), using a voltage-sensitive dye and a photodiode array system. The postsynaptic responses to afferent stimulation first propagated in the stratum opticum and stratum fibrosum et griseum superficiale in an anterograde fashion in the afferents and then expanded vertically into the deep layers. This vertical propagation appeared to occur along a bundle-like structure that corresponded well with a cluster of neurons whose somata are located in the stratum periventriculare. Pharmacological studies showed that these postsynaptic responses were mediated by ionotropic glutamate receptors. On the other hand, the optical signals appeared to consist of at least two components (a transient signal and a slow signal). The second transient signal summated with the first slow signal by paired stimulation, suggesting that the transient and slow signals originated from different cell types. Taken together, these results showed that the functional synaptic organization of the teleost optic tectum comprises of two depolarization-signal propagating paths along a horizontal layer structure and a vertical bundle-like structure and that these synaptic responses occur via glutamatergic transmission.

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