Visual pigments of the tree shrew (Tupaia belangeri) and greater galago (Galago crassicaudatus): A microspectrophotometric investigation

doi:10.1016/0042-6989(90)90053-N

Vision Research

Volume 30, Issue 6, 1990, Pages 839-851

https://doi.org/10.1016/0042-6989(90)90053-N Get rights and content

Abstract

Optical density, linear dichroism and bleaching difference spectra were measured in photoreceptors from the cone-dominated retina of the tree shrew (Tupaia belangeri) and from the rod-dominated retina of the greater galago (Galago crassicaudatus) using a single-beam, wavelength-scanning, dichroic microspectrophotometer. In Tupaia, we obtained spectral records from 272 cone receptors (from 10 eyes), of which 264 were long-wave sensitive (λ_max = 555 ± 6 nm) and 8 were short-wave sensitive (λ_max = 428 ± 15 nm). Also, one anatomically-recognizable rod receptor was encountered and showed a peak absorption at approx. 496 nm. No mid-wave sensitive cone pigment was found, as would be expected in deutan-type dichromats like the tree shrew. Pre-retinal absorption by the cornea and lens was maximal at 370 nm and negligible beyond 430 nm. In Galago, all outer segments measured were rod-like in appearance (λ_max near 501 nm). Measurements of pre-retinal absorption yielded a single-peaked function with a maximum at 363 nm.

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The effects of ambient narrowband long-wavelength light on lens-induced myopia and form-deprivation myopia in tree shrews
2023, Experimental Eye Research
Here we examine the effects of ambient red light on lens-induced myopia and diffuser-induced myopia in tree shrews, small diurnal mammals closely related to primates. Starting at 24 days of visual experience (DVE), seventeen tree shrews were reared in red light (624 ± 10 or 634 ± 10 nm, 527–749 human lux) for 12–14 days wearing either a -5D lens (RL-5D, n = 5) or a diffuser (RLFD, n = 5) monocularly, or without visual restriction (RL-Control, n = 7). Refractive errors and ocular dimensions were compared to those obtained from tree shrews raised in broad-spectrum white light (WL-5D, n = 5; WLFD, n = 10; WL Control, n = 7). The RL-5D tree shrews developed less myopia in their lens-treated eyes than WL-5D tree shrews at the end of the experiment (−1.1 ± 0.9D vs. −3.8 ± 0.3D, p = 0.007). The diffuser-treated eyes of the RLFD tree shrews were near-emmetropic (−0.3 ± 0.6D, vs. −5.4 ± 0.7D in the WLFD group). Red light induced hyperopia in control animals (RL-vs. WL-Control, +3.0 ± 0.7 vs. +1.0 ± 0.2D, p = 0.02), the no-lens eyes of the RL-5D animals, and the no-diffuser eyes of the RLFD animals (+2.5 ± 0.5D and +2.3 ± 0.3D, respectively). The refractive alterations were consistent with the alterations in vitreous chamber depth. The lens-induced myopia developed in red light suggests that a non-chromatic cue could signal defocus to a less accurate extent, although it could also be a result of “form-deprivation” caused by defocus blur. As with previous studies in rhesus monkeys, the ability of red light to promote hyperopia appears to correlate with its ability to retard lens-induced myopia and form-deprivation myopia, the latter of which might be related to non-visual ocular mechanisms.
Limited bandwidth short-wavelength light produces slowly-developing myopia in tree shrews similar to human juvenile-onset myopia
2023, Vision Research
Citation Excerpt :
Tree shrews are small diurnal mammals that are very closely related to primates (Janecka et al., 2007). Like most mammals, tree shrews are dichromats, with short and long wavelength sensitive cone types (Petry & Hárosi, 1990). Most (not all) humans are trichromatic, with short, medium, and long wavelength sensitive cones - but there is evidence that, as regards emmetropization, humans are functionally dichromatic with the medium and long wavelength sensitive cone activities pooled to produce a single “longer” wavelength cone signal (Gawne et al., 2021).
During postnatal development, an emmetropization feedback mechanism uses visual cues to modulate the axial growth of eyes so that, with maturation, images of distant objects are in focus on the retina. If the visual cues indicate that the eye has become too long, it generates STOP signals that slow eye elongation. Myopia is a failure of this process where the eye becomes too long. The existing animal models of myopia have been essential in understanding the mechanics of emmetropization but use visual cues that lead to rapidly progressing myopia and don’t match the stimuli that lead to human myopia. Form deprivation removes esssentially all spatial contrast. Minus lens wear accurately guides axial elongation to restore sharp focus: technically it is not a model of myopia! In contrast, childhood myopia involves a slow drift into myopia, even with the presence of clear images. We hypothesize that, in the modern visual environment, STOP signals are present but often are not quite strong enough to prevent myopic progression. Using tree shrews, small diurnal mammals closely related to primates, we have developed an animal model that we propose better represents this situation. We used limited bandwidth light to provide limited chromatic cues for emmetropization that are not quite enough to produce fully effective STOP signaling, resulting in a slow drift into myopia as seen in children. We hypothesize that this animal model of myopia may prove useful in evaluating anti-myopia therapies where form deprivation and minus lens wear would be too powerful.
Tree shrews do not maintain emmetropia in initially-focused narrow-band cyan light
2021, Experimental Eye Research
We asked if emmetropia, achieved in broadband colony lighting, is maintained in narrow-band cyan light that is well focused in the emmetropic eye, but does not allow for guidance from longitudinal chromatic aberrations (LCA) and offers minimal perceptual color cues. In addition, we examined the response to a −5 D lens in this lighting. Seven tree shrews from different litters were initially housed in broad-spectrum colony lighting. At 24 ± 1 days after eye opening (Days of Visual Experience, DVE) they were housed for 11 days in ambient narrow-band cyan light (peak wavelength 505 ± 17 nm) selected because it is in focus in an emmetropic eye. Perceptually, monochromatic light at 505 nm cannot be distinguished from white by tree shrews. While in cyan light, each animal wore a monocular −5 D lens (Cyan −5 D eyes). The fellow eye was the Cyan no-lens eye. Daily awake non-cycloplegic measures were taken with an autorefractor (refractive state) and with optical low-coherence optical interferometry (axial component dimensions). These measures were compared with the values of animals raised in standard colony fluorescent lighting: an untreated group (n = 7), groups with monocular form deprivation (n = 7) or monocular −5 D lens treatment (n = 5), or that experienced 10 days in total darkness (n = 5). Refractive state at the onset of cyan light treatment was low hyperopia, (mean ± SEM) 1.4 ± 0.4 diopters. During treatment, the Cyan no-lens eyes became myopic (−2.9 ± 0.3 D) whereas colony lighting animals remained slightly hyperopic (1.0 ± 0.2 D). Initially, refractions of the Cyan −5 D eyes paralleled the Cyan no-lens eyes. After six days, they gradually became more myopic than the Cyan no-lens eyes; at the end of treatment, the refractions were −5.4 ± 0.3 D, a difference of −2.5 D from the Cyan no-lens eyes. When returned to colony lighting at 35 ± 1 DVE, the no-lens eye refractions rapidly recovered towards emmetropia but, as expected, the refraction of the −5 D eyes remained near −5 D. Vitreous chamber depth in both eyes was consistent with the refractive changes. In narrow-band cyan lighting the emmetropization mechanism did not maintain emmetropia even though the light initially was well focused. We suggest that, as the eyes diverged from emmetropia, there were insufficient LCA cues for the emmetropization mechanism to utilize the developing myopic refractive error in order to guide the eyes back to emmetropia. However, the increased myopia in the Cyan −5 D eyes in the narrow-band light indicates that the emmetropization mechanism nonetheless detected the presence of the lens-induced refractive error and responded with increased axial elongation that partly compensated for the negative-power lens. These data support the conclusion that the emmetropization mechanism cannot maintain emmetropia in narrow-band lighting. The additional myopia produced in eyes with the −5 D lens shows that the emmetropization mechanism responds to multiple defocus-related cues, even under conditions where it is unable to use them to maintain emmetropia.
An opponent dual-detector spectral drive model of emmetropization
2020, Vision Research
In post-natal developing eyes a feedback mechanism uses optical cues to regulate axial growth so as to achieve good focus, a process termed emmetropization. However, the optical cues that the feedback mechanism uses have remained unclear. Here we present evidence that a primary visual cue may be the detection of different image statistics by the short-wavelength sensitive (SWS) and long-wavelength sensitive (LWS) cone photoreceptors, caused by longitudinal chromatic aberration (LCA). We use as a model system the northern tree shrew Tupaia belangeri, diurnal cone-dominated dichromatic mammals closely related to primates. We present an optical model in which the SWS and LWS photoreceptors each represent an image at different levels of defocus. The model posits that an imbalance between SWS and LWS image statistics directs eye growth towards the point at which these image statistics are in balance. Under spectrally broadband (“white”) lighting, the focus of the eye is driven to a target point approximately in the middle of the visible spectrum, which is emmetropia. Calculations suggest that the SWS cone array, despite the sparse number of SWS cones, can plausibly detect the wavelength-dependent differences in defocus and guide refractive development. The model is consistent with the effects of various narrow-band illuminants on emmetropization in tree shrews. Simulations suggest that common artificial light spectra do not interfere with emmetropization. Simulations also suggest that multi-spectral multi-focal lenses, where the different optical zones of a multifocal lens have different spectral filtering properties, could be an anti-myopia intervention.
The hyperopic effect of narrow-band long-wavelength light in tree shrews increases non-linearly with duration
2018, Vision Research
Citation Excerpt :
Tree shrew retinas contain long wavelength sensitive (LWS “red”, peak absorption at 555 ± 6 nm spectral width at half absorbance) and short wavelength sensitive (SWS “blue”, peak absorption 428 ± 15 nm spectral width at half absorbance) cones (Petry & Harosi, 1990). As shown in Fig. 1A, the light provided by the LEDs was far removed from the SWS-cone absorption peak (Petry & Harosi, 1990). The calculated absorption of the emitted wavelengths was between 6 and 7 log units below the SWS cone peak.
During postnatal refractive development, an emmetropization mechanism uses refractive error to modulate the growth rate of the eye. Hyperopia (image focused behind the retina) produces what has been described as “GO” signaling that increases growth. Myopia (image focused in front of the retina) produces “STOP” signaling that slows growth. The interaction between GO and STOP conditions is non-linear; brief daily exposure to STOP counteracts long periods of GO. In young tree shrews, long-wavelength (red) light, presented 14 h per day, also appears to produce STOP signals. We asked if red light also shows temporal non-linearity; does brief exposure slow the normal decrease in hyperopia in infant animals? At 11 days after eye opening (DVE), infant tree shrews (n = 5/group) began 13 days of daily treatment (red LEDs, 624 ± 10 or 636 ± 10 nm half peak intensity bandwidth) at durations of 0 h (normal animals, n = 7) or 1, 2, 4, or 7 h. Following each daily red period, colony lighting resumed. A 14 h red group had no colony lights. Refractive state was measured daily; ocular component dimensions at the end of the 13-day red-light period. Even 1 h of red light exposure produced some hyperopia. The average hyperopic shift from normal rose exponentially with duration (time constant 2.5 h). Vitreous chamber depth decreased non-linearly with duration (time constant, 3.3 h). After red treatment was discontinued, refractions in colony lighting recovered toward normal; the initial rate was linearly related to the amount of hyperopia. The red light may produce STOP signaling similar to myopic refractive error.
Long-wavelength (red) light produces hyperopia in juvenile and adolescent tree shrews
2017, Vision Research
Citation Excerpt :
The amount of time that the animals spent in the tube was not recorded but did not appear to differ across groups. The illuminance provided by the red LEDs (Fig. 1C) was very far removed from the SWS cone absorption curve for this dichromatic species (Petry & Harosi, 1990); the effect on the SWS cones was between 5 and 6 log units less than on the LWS cones. Thus, the effect of the red LEDs (regardless of whether the peak wavelength was 624 or 636 nm) was to activate almost exclusively the LWS cones and the retinal neurons that receive red-cone inputs.
In infant tree shrews, exposure to narrow-band long-wavelength (red) light, that stimulates long-wavelength sensitive cones almost exclusively, slows axial elongation and produces hyperopia. We asked if red light produces hyperopia in juvenile and adolescent animals, ages when plus lenses are ineffective. Animals were raised in fluorescent colony lighting (100–300 lux) until they began 13 days of red-light treatment at 11 (n = 5, “infant”), 35 (n = 5, “juvenile”) or 95 (n = 5, “adolescent”) days of visual experience (DVE). LEDs provided 527–749 lux on the cage floor. To control for the higher red illuminance, a fluorescent control group (n = 5) of juvenile (35 DVE) animals was exposed to ∼975 lux. Refractions were measured daily; ocular component dimensions at the start and end of treatment and end of recovery in colony lighting. These groups were compared with normals (n = 7). In red light, the refractive state of both juvenile and adolescent animals became significantly (P < 0.05) hyperopic: juvenile 3.9 ± 1.0 diopters (D, mean ± SEM) vs. normal 0.8 ± 0.1 D; adolescent 1.6 ± 0.2 D vs. normal 0.4 ± 0.1 D. The fluorescent control group refractions (0.6 ± 0.3 D) were normal. In red-treated juveniles the vitreous chamber was significantly smaller than normal (P < 0.05): juvenile 2.67 ± 0.03 mm vs. normal 2.75 ± 0.02 mm. The choroid was also significantly thicker: juvenile 77 ± 4 μm vs. normal 57 ± 3 μm (P < 0.05). Although plus lenses do not restrain eye growth in juvenile tree shrews, the red light-induced slowed growth and hyperopia in juvenile and adolescent tree shrews demonstrates that the emmetropization mechanism is still capable of restraining eye growth at these ages.

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Visual pigments of the tree shrew (Tupaia belangeri) and greater galago (Galago crassicaudatus): A microspectrophotometric investigation

Abstract

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Vision Research

Evolution of the visual system in the early primates

The visual pigments of rods and cones in the rhesus monkey (Macaca mulatto)

Journal of Physiology, London

Microspectrophotometric demonstration of four classes of photoreceptors in an old world primate, Macaca fasciculahs

Journal of Physiology, London

Taxonomic status of tree shrews

Science, New York

The nervous system of the tupaiidae: Its bearing on phyletic relationships

The galago visual system: Aspects of normal organization and developmental plasticity

The spectral clustering of visual pigments

Vision Research

Anatomical, electrophysiological and pigmentary aspects of vision in the bush baby: An interpretative study

Vision Research

Human visual pigments: Microspectrophotometric results from the eyes of seven persons

Density and central projections of retinal ganglion cells in the tree shrew

Neuroscience Abstracts

Staining of blue sensitive cones of the macaque retina by a fluorescent dye

Science, New York

Comparative studies upon the eyes of nocturnal lemuroids, monkeys and man

Anatomical Record

Structure and postnatal development of photoreceptors and their synapses in the retina of the tree shrew (Tupaia belangeri)

Cell and Tissue Research

An anatomical and electrophysiological study of the retina of the owl monkey, Aoytus trivirgatus

Journal of Comparative Neurology

Absorption spectra and linear dichroism of some amphibian photoreceptors

Journal of General Physiology

Recent results from single-cell microspectrophotometry: Cone pigments in frog, fish and monkey

Color Research and Application

Cynomolgus and rhesus monkey visual pigments: Application of Fourier transform smoothing and statistical techniques to the determination of spectral parameters

Journal of General Physiology

Dichroic microspectrophotometer: A computer-assisted, rapid, wavelength-scanning photometer for measuring linear dichroism in single cells

Journal of the Optical Society of America

The response range of the blue-cone pathways: A source of vulnerability to disease

Investigative Ophthalmology and Visual Science

The tree shrew retina: Photoreceptors and retinal pigment epithelium