Connectivity of cone photoreceptor telodendria in the zebrafish retina

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The first synapse of the vertebrate visual system relays information from the photoreceptors to bipolar cells, and is serviced by horizontal cells that connect laterally among these adjacent synapses. The latter provides feedback among the neighboring photoreceptors, which enables the comparison and amplification of signals to improve resolution of visual stimuli and detection of their various characters such as edges, sizes, and movements. Similarly, such feedback underpins comparison between spectral subclasses of cones and enables discrimination of wavelengths and color constancy. The mechanisms of this lateral inhibition continue to be debated (Thoreson & Mangel, 2012; Vroman, Klaassen, & Kamermans, 2013; Warren, Van Hook, Tranchina, & Thoreson, 2016). Perhaps prior to this remarkable first synapse, however, adjacent photoreceptors are also coupled directly via telodendria. Telodendria are projections that originate from the photoreceptor pedicle and form gap junctions with other photoreceptors (Kolb, 1977; Li, Chuang, & O'Brien, 2009; O'Brien, Chen, Macleish, O'Brien, & Massey, 2012; O'Brien, Nguyen, & Mills, 2004). Considering the vast and celebrated literature describing the morphology and connectivity of the outer retina, it is notable how little attention has been given to the role(s) of photoreceptor telodendria. The lack of attention regarding telodendria is likely due to the technical difficulty in defining their morphology among the many cellular processes that appear in ultrastructural analysis. Regardless, the pattern of direct coupling between photoreceptors, and whether it might serve to differentially couple certain photoreceptor subtypes, is expected to substantially impact the initial steps of visual signal processing.
Telodendria were first observed in the human retina, and noted to be a common feature of photoreceptors in the 19th century (Cajal, 1893; Schultze, 1866). Since then, photoreceptor telodendria have been reported in many vertebrates, such as reptiles (Baylor, Fuortes, & O'Bryan, 1971; Copenhagen & Owen, 1976a; Detwiler & Hodgkin, 1979; Firsov & Green, 1998; Goede & Kolb, 1995; Kolb & Jones, 1984; Normann, Perlman, Kolb, Jones, & Daly, 1984; Ohtsuka & Kawamata, 1990; Owen, 1985), amphibians (Custer, 1973; Gold & Dowling, 1979; Zhang & Wu, 2004), fish (Hess, Melzer, & Smola, 2002; Kraft & Burkhardt, 1986; Li et al., 2009; O'Brien et al., 2004; Stell, 1972), and mammals (Ahnelt, Keri, & Kolb, 1990; DeVries, Qi, Smith, Makous, & Sterling, 2002; Kolb, 1977; Kolb & West, 1977; Smith, Freed, & Sterling, 1986), including non‐human primates (Hornstein, Verweij, Li, & Schnapf, 2005; O'Brien et al., 2012; Raviola & Gilula, 1975). It was noted that these photoreceptor projections were forming gap junctions with their targets based on inferences from ultrastructural analysis, the presence of connexin, and electrophysiological assessment, suggesting that photoreceptors are indeed using these processes to communicate with other photoreceptors (Baylor et al., 1971; Copenhagen & Owen, 1976a; Detwiler & Hodgkin, 1979; DeVries et al., 2002; Kolb, 1977; Kolb & Jones, 1984; Kolb & West, 1977; Kraft & Burkhardt, 1986; Li et al., 2009; Normann, Perlman, & Daly, 1985; Normann et al., 1984; O'Brien et al., 2004; Owen, 1985; Raviola & Gilula, 1975; Smith et al., 1986; Zhang & Wu, 2004). The function of telodendrial connections remains ambiguous, though they are speculatively thought to improve cone sensitivity and play a role in specific light situations (such as crepuscular vision) to reduce background and increase visual acuity (DeVries et al., 2002; Hornstein et al., 2005; O'Brien et al., 2012; Smith et al., 1986) and reduce signal‐to‐noise (Attwell, Wilson, & Wu, 1985; Gold & Dowling, 1979; Lamb & Simon, 1976).
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