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The Journal of Neuroscience, June 6, 2007, 27(23):6261-6267; doi:10.1523/JNEUROSCI.5646-06.2007

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Behavioral/Systems/Cognitive
A Novel Connection between Rods and ON Cone Bipolar Cells Revealed by Ectopic Metabotropic Glutamate Receptor 7 (mGluR7) in mGluR6-Deficient Mouse Retinas

Yoshihiko Tsukamoto,¹ Katsuko Morigiwa,³ Masaaki Ishii,^1,2 Motoharu Takao,⁴ Ken Iwatsuki,⁵ Shigetada Nakanishi,⁶ and Yutaka Fukuda⁷

¹Departments of Biology and ²Ophthalmology, Hyogo College of Medicine, Nishinomiya, Hyogo 663-8501, Japan, ³EW 89 Synchronicity Research Institute, Tokyo 103-0027, Japan, ⁴Department of Human and Information Science, Tokai University, Hiratsuka, Kanagawa 259-1292, Japan, ⁵Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029, ⁶Osaka Bioscience Institute, Suita, Osaka 565-0874, Japan, and ⁷Department of Physiology, Osaka University Graduate School of Medicine, Suita, Osaka 565-0871, Japan

Correspondence should be addressed to Yoshihiko Tsukamoto, Depatment of Biology, Hyogo College of Medicine, 1-1, Mukogawa, Nishinomiya, Hyogo 663-8501, Japan. Email: ytsuka{at}hyo-med.ac.jp

Since the discovery of direct chemical synapses between rod photoreceptor and OFF cone bipolar cells in mouse retinas, whether the ON cone bipolar cell also receive direct chemical input from rod has been a pending question. In finding that metabotropic glutamate receptor 7 (mGluR7) was uniquely expressed in dendrites of ON cone bipolar cells in the mGluR6-deficient mouse retina, we used this ectopic mGluR7 immunoreactivity as a specific marker for the ON cone bipolar to search for its rod connection. Here, we show that a certain type of ON cone bipolar cell forms ribbon-associated synapses not only with cones, but also rods. This finding was verified in the wild-type mouse retina by three-dimensional reconstruction of bipolar cells from serial electron micrographs. These ON cone bipolars were further identified as corresponding to type 7 of mouse bipolar cell described by Ghosh et al. (2004) and also to the green fluorescent protein (GFP)-labeled type 7 bipolars in the -gustducin-GFP transgenic mouse. Our findings suggest that, in mice, rod signals bifurcate into a third ON and OFF pathway in addition to the two known routes to cone bipolar cells: (1) via rod chemical synapse rod bipolar AII amacrine ON and OFF cone bipolar cells; (2) via rod–cone gap junction cone chemical synapse ON and OFF cone bipolar cells; and (3) via rod chemical synapse ON and OFF cone bipolar cells. This third novel pathway is thought to transmit fast and moderately light-sensitive rod signals, functioning to smooth out the intensity changes at the scotopic–mesopic interface.

Key words: cone; glutamate receptor; network; neurotransmission; retina; rod; vision

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Received Dec. 30, 2006; revised April 19, 2007; accepted May 4, 2007.

Correspondence should be addressed to Yoshihiko Tsukamoto, Depatment of Biology, Hyogo College of Medicine, 1-1, Mukogawa, Nishinomiya, Hyogo 663-8501, Japan. Email: ytsuka{at}hyo-med.ac.jp

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