The wavelength composition and temporal modulation of ambient lighting strongly affect refractive development in young tree shrews

Abstract

Shortly after birth, the eyes of most animals (including humans) are hyperopic because the short axial length places the retina in front of the focal plane. During postnatal development, an emmetropization mechanism uses cues related to refractive error to modulate the growth of the eye, moving the retina toward the focal plane. One possible cue may be longitudinal chromatic aberration (LCA), to signal if eyes are getting too long (long [red] wavelengths in better focus than short [blue]) or too short (short wavelengths in better focus). It could be difficult for the short-wavelength sensitive (SWS, “blue”) cones, which are scarce and widely spaced across the retina, to detect and signal defocus of short wavelengths. We hypothesized that the SWS cone retinal pathway could instead utilize temporal (flicker) information. We thus tested if exposure solely to long-wavelength light would cause developing eyes to slow their axial growth and remain refractively hyperopic, and if flickering short-wavelength light would cause eyes to accelerate their axial growth and become myopic. Four groups of infant northern tree shrews (Tupaia glis belangeri, dichromatic mammals closely related to primates) began 13 days of wavelength treatment starting at 11 days of visual experience (DVE). Ambient lighting was provided by an array of either long-wavelength (red, 626±10 nm) or short-wavelength (blue, 464±10 nm) light-emitting diodes placed atop the cage. The lights were either steady, or flickering in a pseudo-random step pattern. The approximate mean illuminance (in human lux) on the cage floor was red (steady, 527 lux; flickering, 329 lux), and blue (steady, 601 lux; flickering, 252 lux). Refractive state and ocular component dimensions were measured and compared with a group of age-matched normal animals (n=15 for refraction (first and last days); 7 for ocular components) raised in broad spectrum white fluorescent colony lighting (100-300 lux). During the 13 day period, the refraction of the normal animals decreased from (mean±SEM) 5.8±0.7 diopters (D) to 1.5±0.2 D as their vitreous chamber depth increased from 2.77±0.01mm to 2.80±0.03 mm. Animals exposed to red light (both steady and flickering) remained hyperopic throughout the treatment period so that the eyes at the end of wavelength treatment were significantly hyperopic (7.0±0.7 D, steady; 4.7±0.8 D, flickering) compared with the normal animals (p<0.01). The vitreous chamber of the steady red group (2.65±0.03 mm) was significantly shorter than normal (p<0.01). On average, steady blue light had little effect; the refractions paralleled the normal refractive decrease. In contrast, animals housed in flickering blue light increased the rate of refractive decrease so that the eyes became significantly myopic (−2.9±1.3 D) compared with the normal eyes and had longer vitreous chambers (2.93±0.04 mm). Upon return to colony lighting, refractions in all groups gradually returned toward emmetropia. These data are consistent both with the hypothesis that LCA can be an important visual...

In Vivo Imaging of the Retina, Choroid, and Optic Nerve Head in Guinea Pigs

“…The LenStar biometer uses optical low coherence reflectometry to determine corneal thickness, anterior chamber depth, lens thickness and axial length. Although LenStar is calibrated for measurement of ocular dimensions in human eyes, its use has been reported in much smaller eyes such as tree shrews, 49, 50 and as reported in these studies, the ocular dimensions of tree shrews are comparable to guinea pig eyes. Since guinea pig eyes are much smaller than human eyes, the short eye mode in the biometer was used so that consistent peaks for the four refractive surfaces (cornea, anterior and posterior lens and retina) were visible (Figure 2A).…”

“…Although LenStar is calibrated for measuring axial dimensions in human eyes, its use for measurement of axial dimensions has been previously reported in smaller eyes, including those of tree shrews, which have ocular dimensions similar to that of guinea pigs. 49, 50 In the chick eye, Penha, et al, report high correlation for anterior chamber depth, vitreous chamber depth, and axial length, with only a 0.5 mm difference in axial length between A-scan ultrasound and optical low-coherence tomography. 59 Here, we measured enucleated globes and isolated lenses against a ruler under a dissecting microscope, and found the measurements were similar to those from the LenStar.…”

Long-wavelength (red) light produces hyperopia in juvenile and adolescent tree shrews

“…1A). The animals in the 11 DVE group were included in a previous study (Gawne, Siegwart et al 2017). The 11 DVE group was at an age when tree shrews will respond to a plus lens; the 35 DVE group was past the age when tree shrews stop responding to plus lenses (Siegwart and Norton 2010, Guo, Frost et al 2012); the 95 DVE group was nearing sexual maturity (comparable to human adolescents).…”

“…The three experimental and the fluorescent control groups were compared with a normal group (n=7) that was exposed to only standard fluorescent colony lighting (100 to 300 lux) for 14 hours a day throughout development, and was derived from previous experiments (Ward, Siegwart et al 2016, Gawne, Siegwart et al 2017). …”

“…In infant tree shrews (dichromatic mammals closely related to primates) (Luckett 1980) we have recently found that narrow-band red light, that only stimulates the LWS cones, produces slowed axial elongation and prevents the normal decrease in refraction from hyperopia to emmetropia so that the eyes remain substantially hyperopic (Gawne, Siegwart et al 2017). Similar results have been found in infant monkeys (Smith, Hung et al 2015).…”