The morphological characterization of orientation‐biased displaced large‐field ganglion cells in the central part of goldfish retina

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The vertebrate retina contains about 20–30 subtypes of ganglion cells (Hitchcock & Easter, 1986; Roska & Werblin, 2001; Rockhill, Daly, MacNeil, Brown, & Masland, 2002; Marc & Jones, 2002; Sanes & Masland 2015). Each ganglion cell receives synaptic input from specific types of bipolar and amacrine cells at the same depth of the inner plexiform layer (IPL) and is thought to process a specific aspect of visual information. Therefore, to understand the function of ganglion cells, it is important to identify how the ganglion cells connect to the specific types of bipolar and amacrine cells.
It is also important to determine the lateral wiring patterns connected with neighboring cells via gap junctions, such as those intervening between pairs of amacrine cells, pairs of ganglion cells, and between ganglion and amacrine cells. Among other functions, these gap junctions can enlarge the receptive field of cells (Völgyi, Chheda, & Bloomfield, 2009; Arai, Tanaka, & Tachibana, 2010). Recently, it has been shown that the gap junctional pattern of the different types of ganglion cells in the adult mouse and rabbit retina are different and characteristic of each ganglion cell type (Hoshi, Kim, & Mills, 2007; Völgyi et al., 2009). Most ganglion cell types, around 70%, are tracer‐coupled to neighboring ganglion cells of the same type and/or specific type of amacrine cells. Where tested, these ganglion cells show synchronized firing at intervals characteristic of gap junctions (Levine 1997; Hu & Bloomfield, 2003; Hu, Pan, Völgyi, & Bloomfield, 2010; Ackert et al., 2006). Synchronized oscillations between dimming detector ganglion cells in the frog retina were also shown to contribute to the escape behavior (Ishikane, Gangi, Honda, & Tachibana, 2005). Therefore, the lateral wiring connected with gap junctions in retinal circuits may contribute to the production of such behaviors.
Additionally, it is well established that dopamine modulates gap junctions at many sites in retina (Teranishi, Negishi, & Kato, 1983; DeVries & Schwartz, 1989; Mills & Massey, 1995; Mills et al., 2007; Hu et al., 2010), as well as ganglion cell excitability (Hayashida et al., 2009; Ogata, Stradleigh, Partida, & Ishida, 2012). Moreover, dopamine‐stimulated phosphorylation in AII amacrine cells modulates gating of gap junctions (Kothmann, Massey, & O'Brien, 2009). Therefore, it is important to understand whether dopamine contributes to modulation of gap junctions or of ganglion cell excitability.
Dopamine is extrasynaptically released from the dopaminergic amacrine cells in the mouse retina (Puopolo, Hochstetler, Gustincich, Wightman, & Raviola, 2001; Hirasawa, Puopolo, & Raviola, 2009), and the receptors are widely expressed on many processes in retina (Hayashida et al., 2009), but it is not entirely clear which are primarily stimulated by volume transmission of dopamine (Witkovsky & Dearry, 1991), and which might possibly receive traditional synaptic inputs from closely‐apposed dopaminergic synapses. Dopamine processes have been shown to be closely apposed to some retinal targets, such as the AII amacrine cell somas (Contini & Raviola, 2003), dorsally directed amacrine cells (Hoshi & Mills, 2009), and also melanopsin ganglion cells branched axons (Liao et al. 2016).
So far, however, neither dopamine D1 receptors nor D2 receptors have been demonstrated on the postsynaptic sites between presynaptic dopaminergic amacrine cells and postsynaptic AII amacrine cells (Veruki & Wässle, 1996; Derouiche & Asan, 1999). Recently, however, Uchigashima, Ohtsuka, Kobayashi, and Watanabe (2016) demonstrated that the midbrain dopamine neurons (presynaptic) synapsed onto the medium spiny neurons (postsynaptic) via GABA receptors underneath the synaptic sites, while dopamine receptors were located outside the synaptic sites; perisynaptic (< 100 nm from the edge of dopamine neurons) and extrasynaptic (> 100 nm) membrane.
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