Photoreceptor Development in Premetamorphic and Metamorphic <i>Xenopus laevis</i>

Parker, Ryan; Mccarragher, Brent; Crouch, Rosalie K.; Darden, Alix G.

doi:10.1002/ar.21079

Cited by 7 publications

(6 citation statements)

References 31 publications

(38 reference statements)

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“…The visual stimulation device was custom built by H.X., and consisted of a miniature LCD screen (Kopin Corporation, Taunton, MA, USA), back‐lit with a powerful light emission diode [either red (LXHL‐LD3C), wavelength 645 nm, or blue (LXHL‐LB3C), wavelength 490 nm; Lumileds Lighting, USA; both colors are highly visible for Xenopus tadpoles (Parker et al ., ; Blackiston & Levin, )], and projected by a lens onto one end of a high‐fidelity image fiber (600 μm in diameter) (Fujikura Ltd, Tokyo, Japan). The other end of the fiber was brought to the tadpole's eye, placed at 400–600 μm from the lens of the eye, and centered along the eye axis, covering about 60–100° of the visual field.…”

Section: Methodsmentioning

confidence: 99%

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles

Khakhalin

Koren

et al. 2014

Eur J of Neuroscience

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Information processing in the vertebrate brain is thought to be mediated through distributed neural networks, but it is still unclear how sensory stimuli are encoded and detected by these networks, and what role synaptic inhibition plays in this process. Here we used a collision avoidance behavior in Xenopus tadpoles as a model for stimulus discrimination and recognition. We showed that the visual system of the tadpole is selective for behaviorally relevant looming stimuli, and that the detection of these stimuli first occurs in the optic tectum. By comparing visually guided behavior, optic nerve recordings, excitatory and inhibitory synaptic currents, and the spike output of tectal neurons, we showed that collision detection in the tadpole relies on the emergent properties of distributed recurrent networks within the tectum. We found that synaptic inhibition was temporally correlated with excitation, and did not actively sculpt stimulus selectivity, but rather it regulated the amount of integration between direct inputs from the retina and recurrent inputs from the tectum. Both pharmacological suppression and enhancement of synaptic inhibition disrupted emergent selectivity for looming stimuli. Taken together these findings suggested that, by regulating the amount of network activity, inhibition plays a critical role in maintaining selective sensitivity to behaviorally-relevant visual stimuli.

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Section: Methodsmentioning

confidence: 99%

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles

Khakhalin

Koren

et al. 2014

Eur J of Neuroscience

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“…Mouse monoclonal antibody 4D2 targets amino acids 2 to 39 of the bovine rod opsin N terminus (Hicks and Molday, 1986) and has been widely used to specifically label rod photoreceptors in many vertebrates, including mouse (Linberg et al, 2005), marmoset (Hendrickson et al, 2006), chicken (Fischer et al, 2008), frog (Parker et al, 2010), and salamander (Sherry et al, 1998). In western blots of goldfish rod outer segment homogenate, 4D2 labeled a band at %38 kDa, likely rod opsin (Knight and Raymond, 1990).…”

Section: Immunohistochemistrymentioning

confidence: 97%

Unique photoreceptor arrangements in a fish with polarized light discrimination

Flamarique

2011

J of Comparative Neurology

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In contrast to other vertebrates, some anchovies have cone photoreceptors with longitudinally oriented outer segment lamellae. These photoreceptors are axially dichroic (i.e., they are sensitive to the polarization of axially incident light) and form the basis of a polarization detection system in the northern anchovy, Engraulis mordax. Whether other cone types exist in the retina of this animal, and whether multiple cone opsins are expressed in the retinas of anchovies, is unknown. Likewise, a detailed examination of photoreceptor ultrastructure in nondichroic photoreceptors has not been carried out despite its importance to understand visual specializations within the retina and its use in the formulation of models to explain cellular structure. Here, I combined light and electron microscopy with immunohistochemical studies of opsin expression to infer mechanisms of lamellar formation and to evaluate the potential for color vision in the northern anchovy retina. Morphological observations revealed three cone formations: 1) continuous rows made up of alternating long and short (bilobed) cones with longitudinally oriented lamellae that are orthogonal between cone types; 2) continuous rows of alternating long and short cones in which only the short cones have longitudinally oriented lamellae; and 3) rows of triple cones with transversely oriented lamellae, each triple cone consisting of two lateral cones flanking a small central cone. Ultrastructure investigations supported two models of outer segment formation resulting in the longitudinally oriented lamellae of long and short cones. In the case of the long cone, lateral compression of the outer segment, potentially via the formation of guanine platelet stacks in neighboring pigment epithelium cells, results in a shape transformation from conical to cunate and a tilt from transverse to longitudinal lamellae. In the case of the short (bilobed) cone, membrane invaginations from the connecting ciliary structure grow longitudinally to form a dichroic stack. Opsin expression studies indicated that all cones express middle-to-long wavelength opsins, with long and lateral cones possessing a different opsin from that in short and central cones, confirming the potential for color vision. Together with the ultrastructural observations, these results suggest that the unique cone topography in the northern anchovy retina may underlie a visual system with segregated color and polarization detection channels.

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“…At stage NF48, the higher D3 expression observed in most photoreceptors and in cells of the inner nuclear cell layer, could be related to the fact that retina need to be protected from the step increase in TH levels that will initiate pro-metamorphosis at NF54 [ 31 ]. Pro-metamorphosis is a step where TH signaling is active and T 3 -dependent tissue remodeling starts [ 30 ], illustrated by the onset of green rod differentiation in retina [ 21 ].…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, previous studies in Xenopus retina addressed the question of the regulation of the stem cells and progenitor cells proliferation [ 15 ] or the genesis of different cell types [ 16 , 17 , 18 , 19 ] in early development. Other studies addressed the determination of cone and rod photoreceptors during embryonic stages NF33-41 [ 20 , 21 ]. These studies raised the importance of local environment and extrinsic factors but did not address the role of TH.…”

Section: Introductionmentioning

confidence: 99%

Expression of the inactivating deiodinase, Deiodinase 3, in the pre-metamorphic tadpole retina

Blay¹,

Préau²,

Morvan-Dubois³

et al. 2018

PLoS ONE

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Thyroid hormone (TH) orchestrates amphibian metamorphosis. Thus, this developmental phase is often used to study TH-dependent responses in specific tissues. However, TH signaling appears early in development raising the question of the control of TH availability in specific cell types prior to metamorphosis. TH availability is under strict temporal and tissue-specific control by deiodinases. We examined the expression of the TH-inactivating enzyme, deiodinase type 3 (D3), during early retinal development. To this end we created a Xenopus laevis transgenic line expressing GFP from the Xenopus dio3 promoter region (pdio3) and followed pdio3–GFP expression in pre-metamorphic tadpoles. To validate retinal GFP expression in the transgenic line as a function of dio3 promoter activity, we used in situ hybridization to compare endogenous dio3 expression to reporter-driven GFP activity. Retinal expression of dio3 increased during pre-metamorphosis through stages NF41, 45 and 48. Both sets of results show dio3 to have cell-specific, dynamic expression in the pre-metamorphic retina. At stage NF48, dio3 expression co-localised with markers for photoreceptors, rods, Opsin-S cones and bipolar neurons. In contrast, in post-metamorphic juveniles dio3 expression was reduced and spatially confined to certain photoreceptors and amacrine cells. We compared dio3 expression at stages NF41 and NF48 with TH-dependent transcriptional responses using another transgenic reporter line: THbZIP-GFP and by analyzing the expression of T3-regulated genes in distinct TH availability contexts. At stage NF48, the majority of retinal cells expressing dio3 were negative for T3 signaling. Notably, most ganglion cells were virtually both dio3-free and T3-responsive. The results show that dio3 can reduce TH availability at the cellular scale. Further, a reduction in dio3 expression can trigger fine-tuned T3 action in cell-type specific maturation at the right time, as exemplified here in photoreceptor survival in the pre-metamorphic retina.

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Photoreceptor Development in Premetamorphic and Metamorphic Xenopus laevis

Abstract: Transgenic Xenopus laevis are commonly used to study gene expression in photoreceptors, but only red rods and red cones are known to exist in the pre-metamorphic stages commonly used in transgenic studies.

Cited by 7 publications

References 31 publications

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles

Unique photoreceptor arrangements in a fish with polarized light discrimination

Expression of the inactivating deiodinase, Deiodinase 3, in the pre-metamorphic tadpole retina

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