Abstract
The visual system consists of two major subsystems, image-forming circuits that drive conscious vision and non-image-forming circuits for behaviors such as circadian photoentrainment. While historically considered non-overlapping, recent evidence has uncovered crosstalk between these subsystems. Here, we investigated shared developmental mechanisms. We revealed an unprecedented role for light in the maturation of the circadian clock and discovered that intrinsically photosensitive retinal ganglion cells (ipRGCs) are critical for this refinement process. In addition, ipRGCs regulate retinal waves independent of light, and developmental ablation of a subset of ipRGCs disrupts eye-specific segregation of retinogeniculate projections. Specifically, a subset of ipRGCs, comprising ~200 cells and which project intraretinally and to circadian centers in the brain, are sufficient to mediate both of these developmental processes. Thus, this subset of ipRGCs constitute a shared node in the neural networks that mediate light-dependent maturation of the circadian clock and light-independent refinement of retinogeniculate projections.
Highlights
Light is detected by the eye for image-forming functions, including conscious perception of the visual scene, and for non-image-forming (NIF) functions, such as synchronization of circadian rhythms to the solar day and the pupillary light reflex
Using the LacZ locus with the attenuated diphtheria toxin (aDTA) or diphtheria toxin (DTA) loci, we show that at 6 months of age, about 75 M1 intrinsically photosensitive Research articleNeuroscience ganglion cells (RGCs) (ipRGCs) survived in Opn4LacZ/DTA mice (Supplementary file 1), and consistent with our previous report, about 125 M1 ipRGCs survived in Opn4LacZ/aDTA mice (Guler et al, 2008) (Figure 1F; Supplementary file 1)
These results show that even some ipRGCs that express high levels of melanopsin (M1s) can survive the presence of a single dose of the full strength DTA
Summary
Light is detected by the eye for image-forming functions, including conscious perception of the visual scene, and for non-image-forming (NIF) functions, such as synchronization of circadian rhythms to the solar day (circadian photoentrainment) and the pupillary light reflex. A subset of RGCs, is intrinsically photosensitive (Berson, 2003; Berson et al, 2002; Hattar et al, 2002; Provencio et al, 1998), in addition to receiving indirect light signals from the classical photoreceptors, rods and cones (Lucas et al, 2003; Mrosovsky and Hattar, 2003; Panda et al, 2002; Ruby et al, 2002; Schmidt et al, 2008) These intrinsically photosensitive RGCs (ipRGCs) constitute the sole conduit of light information to non-image-forming centers in the brain, such as the suprachiasmatic nucleus (SCN) (Guler et al, 2008; Hattar et al, 2003; Panda et al, 2003). Reports envisioned a strict separation between the image- and non-image-forming visual networks (Dreher and Robinson, 1991; Moore, 1997; Young and Lund, 1994), but this view has begun to be challenged by recent evidence for functional crosstalk between the two systems (Ecker et al, 2010; Estevez et al, 2012; Renna et al, 2011; Schmidt et al, 2014; Zhang et al, 2008)
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