Disruption of the Centrifugal Visual System Inhibits Early Eye Growth in Chicks

Dillingham, Christopher M.; Guggenheim, Jeremy A.; Erichsen, Jonathan Thor

doi:10.1167/iovs.12-11548

Cited by 13 publications

(20 citation statements)

References 66 publications

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“…In tree shrews (mammals closely related to primates), stimulation of this pathway produces remodeling of the scleral extracellular matrix that alters its biomechanical properties, increasing the viscoelasticity and the axial elongation rate. We will refer to this as the “direct emmetropization pathway” because it can operate, albeit less well, in the absence of an “indirect” pathway comprised of connections from the retina, through central visual structures, that controls accommodation and other potential outputs to the eye and can affect refractive development (Dillingham, Guggenheim, & Erichsen, 2013; McFadden & Wildsoet, 2009; Schaeffel et al, 1990; Wildsoet, 2003). …”

Section: Introductionmentioning

confidence: 99%

Gene expression signatures in tree shrew choroid in response to three myopiagenic conditions

Frost

Siegwart

et al. 2014

Vision Research

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We examined gene expression in tree shrew choroid in response to three different myopiagenic conditions: minus lens (ML) wear, form deprivation (FD), and continuous darkness (DK). Four groups of tree shrews (n = 7 per group) were used. Starting 24 days after normal eye opening (days of visual experience [DVE]), the ML group wore a monocular −5 D lens for 2 days. The FD group wore a monocular translucent diffuser for 2 days. The DK group experienced continuous darkness binocularly for 11 days, starting at 17 DVE. An age-matched normal group was examined at 26 DVE. Quantitative PCR was used to measure the relative (treated eye vs. control eye) differences in mRNA levels in the choroid for 77 candidate genes. Small myopic changes were observed in the treated eyes (relative to the control eyes) of the ML group (−1.0 ± 0.2 D; mean ± SEM) and FD group (−1.9 ± 0.2 D). A larger myopia developed in the DK group (−4.4 ± 1.0 D) relative to Normal eyes (both groups, mean of right and left eyes). In the ML group, 28 genes showed significant differential mRNA expression; eighteen were down-regulated. A very similar pattern occurred in the FD group; twenty-seven of the same genes were similarly regulated, along with five additional genes. Fewer expression differences in the DK group were significant compared to normal or the control eyes of the ML and FD groups, but the pattern was similar to that of the ML and FD differential expression patterns. These data suggest that, at the level of the choroid, the gene expression signatures produced by “GO” emmetropization signals are highly similar despite the different visual conditions.

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Section: Introductionmentioning

confidence: 99%

Gene expression signatures in tree shrew choroid in response to three myopiagenic conditions

Frost

Siegwart

et al. 2014

Vision Research

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“…It is important to note that severing the optic nerve disrupts not only the efferents of RGCs to the primary visual centers of the brain but also the axons of the CVS that terminate within the retina. We have previously reported that disruption of centrifugal neurons, while preserving retinal ganglion cell axons, has comparable effects to those reported following optic nerve section: both manipulations result in vitreous chamber-dependent hyperopia (Troilo et al 1987; Wildsoet and Wallman 1995; Wildsoet 2003; Dillingham et al 2013). Specifically, following disruption of centrifugal axons but leaving RGC axons within the optic nerve intact, chicks developed an initial hyperopia in the eye contralateral to the lesion.…”

Section: Introductionmentioning

confidence: 63%

“…One group of chicks ( n = 8) was used to assess the normal, strain-specific baseline ocular growth pattern under constant light conditions ( n = 8), i.e., these chicks did not undergo surgery to disrupt centrifugal efferents, for comparison with the ocular growth pattern of chicks of the same strain raised under normal diurnal light conditions (14 h light, 10 h dark cycle; data taken from a control group of 14 chicks in a previous, related study; Dillingham et al 2013). Subsequently, a second age-matched group ( n = 17) either underwent stereotaxic surgery to perform a unilateral electrolytic lesion of the IOTr or ION, in order to disrupt centrifugal neurons to the retina ( n = 12; Fig.…”

Section: Methodsmentioning

confidence: 99%

“…Specifically, following disruption of centrifugal axons but leaving RGC axons within the optic nerve intact, chicks developed an initial hyperopia in the eye contralateral to the lesion. Crucially, however, unlike the persistent disruption of emmetropization observed following optic nerve section, emmetropia was re-established by the end of the 3-week observation period (Dillingham et al 2013). …”

Section: Introductionmentioning

confidence: 99%

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The effect of unilateral disruption of the centrifugal visual system on normal eye development in chicks raised under constant light conditions

2016

Self Cite

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The centrifugal visual system (CVS) comprises a visually driven isthmic feedback projection to the retina. While its function has remained elusive, we have previously shown that, under otherwise normal conditions, unilateral disconnection of centrifugal neurons in the chick affected eye development, inducing a reduced rate of axial elongation that resulted in a unilateral hyperopia in the eye contralateral to the lesion. Here, we further investigate the role of centrifugal neurons in ocular development in chicks reared in an abnormal visual environment, namely constant light. The baseline ocular phenotype of constant light-reared chicks (n = 8) with intact centrifugal neurons was assessed over a 3-week post-hatch time period and, subsequently, compared to chicks raised in normal diurnal lighting (n = 8). Lesions of the isthmo-optic tract or sham surgeries were performed in another seventeen chicks, all raised under constant light. Ocular phenotyping was performed over a 21-day postoperative period to assess changes in refractive state (streak retinoscopy) and ocular component dimensions (A-scan ultrasonography). A pathway-tracing paradigm was employed to quantify lesion success. Chicks raised in constant light conditions with an intact CVS developed shallower anterior chambers combined with elongated vitreous chambers relative to chicks raised in normal diurnal lighting. Seven days following surgery to disrupt centrifugal neurons, a significant positive correlation between refractive error asymmetry between the eyes and lesion success was evident, characterized by hyperopia in the eye contralateral to the lesion. By 21 days post-surgery, these contralateral eyes had become emmetropic, while ipsilateral eyes had developed relative axial hyperopia. Our results provide further support for the hypothesis that the centrifugal visual system can modulate eye development.

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“…Centrifugal fibers arising in the Edinger-Westfal nucleus are responsible for visual acuity [49]. After the lesion of the tecto-fugal pathway there is deficit in the color reversal-learning [63,64]. The retinopetal pathway arising in the serotoninergic raphe nuclei can enhance phase shift of the circadian rhythm to light [51].…”

Section: Functional Considerationsmentioning

confidence: 99%

Recent Research on the Centrifugal Visual System in Mammalian Species

Köves¹,

Csáki²,

Vereczki³

2016

Anat Physiol

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Ample evidence indicates that both retinofugal (classical visual and the retino-hypothalamic pathways) and retinopetal connections (centrifugal visual system) are found between the eye and the central nervous system. More than hundred years ago Ramon Y Cajal and Dogiel, whose names are very well known by neuro-anatomists, described the termination pattern of the fibers deriving from the avian central nervous system. However, the location of nerve cell bodies was not known at that time. In the last century many data accumulated about these neurons not only in lower vertebrates but in mammals as well. The structures where the neurons give rise to the centrifugal visual fibres in mammals are the following: reticular formation and raphe nuclei of the midbrain, superior colliculus, pretectum, gray matter of the midbrain, dentate gyrus, CA1 and CA3 regions of the hippocampus, olfactory tubercle, habenula, indusium griseum, hypothalamic supraoptic, Paraiventricular and arcuate nuclei, and the lateral hypothalamus. The centrifugal visual fibers enter the optic nerve layer, then reach the inner plexiform layer and terminate in the inner nulear layer of the retina in the vicinity of the amacrine cells. A series of neuropeptides and neurotransmitters was described in the origin of the centrifugal visual system. These are the followings: luteinizing hormone releasing hormone, pituitary adenylate cyclase activating polypeptide, vasoactive intestinal polypeptide, serotonin, histamine and leu-enkephalin. Several hypotheses arose on the function of this system. Centrifugal visual system arising from the histaminergic mammillary neurons modifies the sleep/wake cycle. Hallucinogenic drugs through the limbic system may cause disturbance of visual function and result in seeing visual hallucinations or distorted images.

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Disruption of the Centrifugal Visual System Inhibits Early Eye Growth in Chicks

Abstract: Unilateral disruption of centrifugal efferents to the retina of the contralateral eye induces an initial axial hyperopia, which is subsequently reversed through increased vitreous elongation in the affected eyes.

Cited by 13 publications

References 66 publications

Gene expression signatures in tree shrew choroid in response to three myopiagenic conditions

Gene expression signatures in tree shrew choroid in response to three myopiagenic conditions

The effect of unilateral disruption of the centrifugal visual system on normal eye development in chicks raised under constant light conditions

Recent Research on the Centrifugal Visual System in Mammalian Species

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