Subtype-dependent postnatal development of direction- and orientation-selective retinal ganglion cells in mice

Chen, Hui; Liu, Xiaorong; Tian, Na

doi:10.1152/jn.00320.2014

Cited by 31 publications

(34 citation statements)

References 43 publications

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Section: Author Manuscriptsupporting

confidence: 77%

“…We found no significant difference for the DSIs of either ON and ON-OFF DSGCs across conditions [3,6], and a small but significant increase in the vector sum for ON-OFF DSGCs across development, as described previously [5,8], suggesting a visually-driven maturation of tuning properties. Though DSGCs were strongly tuned at eye-opening and after darkrearing, both ON and ON-OFF DSGCs in young and dark-reared mice retained the immature distribution of preferred directions, failing to cluster along the cardinal axes ( Figure 2; Figure S2).…”

Section: Clustering Of Dsgc Preferred Directions Along Cardinal Axes supporting

confidence: 76%

“…How these preferred directions emerge during development is still not understood. Several studies have demonstrated that ON [2] and ON-OFF DSGCs are well tuned at eye-opening, and even a few days prior to eye-opening, in rabbits [3], rats [4] and mice [5][6][7][8], suggesting that visual experience is not required to produce direction selective tuning. However, here we show that at eye-opening the preferred directions of both ON and ON-OFF DSGCs are diffusely distributed and that visual deprivation prevents the preferred directions from clustering along the cardinal axes.…”

Section: Discussionmentioning

confidence: 99%

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Role for Visual Experience in the Development of Direction-Selective Circuits

Bos¹,

Gainer²,

Feller³

2017

Current Biology

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SUMMARYVisually-guided behavior can depend critically on detecting the direction of object movement. This computation is first performed in the retina where direction is encoded by direction-selective ganglion cells (DSGCs) that respond strongly to an object moving in the preferred direction and weakly to an object moving in the opposite, or null, direction (reviewed in [1]). These DSGCs come in multiple types that are classified based on their morphologies, response properties and targets in the brain. This study focuses on two types -ON and ON-OFF DSGCs. Though animals can sense motion in all directions, the preferred directions of DSGCs in adult retina cluster along distinct directions that we refer to as the cardinal axes. ON DSGCs have three cardinal axestemporal, ventral and dorsonasal -while ON-OFF DSGCs have four -nasal, temporal, dorsal, and ventral. How these preferred directions emerge during development is still not understood. Several studies have demonstrated that ON [2] and ON-OFF DSGCs are well tuned at eye-opening, and even a few days prior to eye-opening, in rabbits [3], rats [4] and mice [5][6][7][8], suggesting that visual experience is not required to produce direction selective tuning. However, here we show that at eye-opening the preferred directions of both ON and ON-OFF DSGCs are diffusely distributed and that visual deprivation prevents the preferred directions from clustering along the cardinal axes. Our findings indicate a critical role for visual experience in shaping responses in the retina. HHS Public Access RESULTS Clustering of DSGC preferred directions along cardinal axes after eye-opening requires visual experienceWe used two-photon calcium imaging to study the development of DSGC populations in mouse retina. This imaging technique has proven to be quite powerful in characterizing the receptive field properties of retinal ganglion cells [9][10][11][12]. We loaded retinas of WT mice near eye-opening (P13-P14) and in adulthood (>P30) with the calcium dye Oregon green 488 BAPTA-1 hexapotassium salt (OGB-1) via electroporation, thus uniformly labeling the ganglion cell layer ( Figure 1A; see Supplemental Information). Ventral portions of the retina were stimulated with light centered at 385 nm to maximally activate UV-cones [13,14] while minimizing cross talk with the imaging detectors ( Figure S1). This approach allowed us to record from all DSGC subtypes within a single field of view (~40000 μm 2 ).To identify DSGCs, we first used full field UV-light flashes to classify cells as ON, OFF or ON-OFF retinal ganglion cells (RGCs) ( Figure S1; Table S1). We found that around 80% of the cells in the ganglion cell layer of young and adult retinas responded to light flashes with changes in fluorescence (Table S1), similar to the RGC percentages reported in previous studies [9,11,12]. In addition, over development we observed a decrease in the percentage of ON-OFF RGCs (28.03% at P13-14 to 20.84% in adult) (Table S1) [15].Second, we used light bars on a dark background drifting in 8 dir...

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Section: Author Manuscriptsupporting

confidence: 77%

Section: Clustering Of Dsgc Preferred Directions Along Cardinal Axes supporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

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Role for Visual Experience in the Development of Direction-Selective Circuits

Bos¹,

Gainer²,

Feller³

2017

Current Biology

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“…1C-F ). Recordings were conducted in the ventral retina, where there is a higher concentration of S-cones versus M-cones due to the gradient distribution of opsins in the mouse retina (Wang et al, 2011;Baden et al, 2013;Hoon et al, 2014) (Fig. 1C).…”

Section: Methodsmentioning

confidence: 99%

“…In Gnat1 Ϫ/Ϫ mice, visible light evoked responses only at the highest light intensities, indicating activation of M-cones that are present at a lower density in ventral than dorsal retina (Wang et al, 2011;Baden et al, 2013). This was verified as being an M-cone-mediated response by obtaining a similar response threshold after sustained exposure of WT retinas to green light generated by placing a green filter over the microscope condenser (ϳ1.6 ϫ 10 6 R*/rod/s for at least 2 min as used in Wang et al, 2011; data not shown).…”

Section: Methodsmentioning

confidence: 99%

Contributions of Rod and Cone Pathways to Retinal Direction Selectivity Through Development

et al. 2016

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Direction selectivity is a robust computation across a broad stimulus space that is mediated by activity of both rod and cone photoreceptors through the ON and OFF pathways. However, rods, S-cones, and M-cones activate the ON and OFF circuits via distinct pathways and the relative contribution of each to direction selectivity is unknown. Using a variety of stimulation paradigms, pharmacological agents, and knockout mice that lack rod transduction, we found that inputs from the ON pathway were critical for strong direction-selective (DS) tuning in the OFF pathway. For UV light stimulation, the ON pathway inputs to the OFF pathway originated with rod signaling, whereas for visible stimulation, the ON pathway inputs to the OFF pathway originated with both rod and M-cone signaling. Whole-cell voltageclamp recordings revealed that blocking the ON pathway reduced directional tuning in the OFF pathway via a reduction in null-side inhibition, which is provided by OFF starburst amacrine cells (SACs). Consistent with this, our recordings from OFF SACs confirmed that signals originating in the ON pathway contribute to their excitation. Finally, we observed that, for UV stimulation, ON contributions to OFF DS tuning matured earlier than direct signaling via the OFF pathway. These data indicate that the retina uses multiple strategies for computing DS responses across different colors and stages of development.Key words: development; direction selectivity; direction selective ganglion cells; Gnat1; retina; rod/cone pathway IntroductionOne of the remarkable properties of the retina is its ability to encode visual features for both ON and OFF polarity in light intensities that vary across several orders of magnitude and spectral content. For example, direction-selective ganglion cells (DSGCs), which fire strongly when an object moves in the preferred direction (PD) and fire minimally when the object moves in the opposite (null) direction (ND) (Fig. 1B), show similar tuning across different light intensities (Hoggarth et al., 2015). Responses across light conditions are mediated by different classes of photoreceptors: rod photoreceptors are active at low light levels, whereas S-cone and M-cone photoreceptors become active at bright light levels. In the mouse retina, rod-mediated signaling also contributes to visual processing in intermediate and bright light conditions (Ke et al., 2014; Szikra et al., 2014; Vlasits et al., 2014;Grimes et al., 2015;Tikidji-Hamburyan et al., 2015; Joesch and Meister, 2016), indicating that a complex set of interactions between rod and cone pathways influence the encoding features of the retina.Cones and rods feed into circuits that are initially distinct in the outer retina, but then converge onto the same cell types in the inner retina (Fig. 1A). Cones synapse onto two major subtypes of cone bipolar cells (cBCs): ON cBCs that depolarize in response to increases in light and OFF cBCs that depolarize in response to deReceived Oct. 19, 2015; revised July 11, 2016; accepted July 28, 2016 Significa...

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Differential effects of experimental glaucoma on intrinsically photosensitive retinal ganglion cells in mice

Gao

Griner

Liu

et al. 2022

J of Comparative Neurology

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Glaucoma is a group of eye diseases characterized by retinal ganglion cell (RGC) loss and optic nerve damage. Studies, including this study, support that RGCs degenerate and die in a type‐specific manner following the disease insult. Here we specifically examined one RGC type, the intrinsically photosensitive retinal ganglion cell (ipRGC), and its associated functional deficits in a mouse model of experimental glaucoma. We induced chronic ocular hypertension (OHT) by laser photocoagulation and then characterized the survival of ipRGC subtypes. We found that ipRGCs suffer significant loss, similar to the general RGC population, but ipRGC subtypes are differentially affected following chronic OHT. M4 ipRGCs, which are involved in pattern vision, are susceptible to chronic OHT. Correspondingly, mice with chronic OHT experience reduced contrast sensitivity and visual acuity. By comparison, M1 ipRGCs, which project to the suprachiasmatic nuclei to regulate circadian rhythmicity, exhibit almost no cell loss following chronic OHT. Accordingly, we observed that circadian re‐entrainment and circadian rhythmicity are largely not disrupted in OHT mice. Our study demonstrates the link between subtype‐specific ipRGC survival and behavioral deficits in glaucomatous mice. These findings provide insight into glaucoma‐induced visual behavioral deficits and their underlying mechanisms.

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Subtype-dependent postnatal development of direction- and orientation-selective retinal ganglion cells in mice

Cited by 31 publications

References 43 publications

Role for Visual Experience in the Development of Direction-Selective Circuits

Role for Visual Experience in the Development of Direction-Selective Circuits

Contributions of Rod and Cone Pathways to Retinal Direction Selectivity Through Development

Differential effects of experimental glaucoma on intrinsically photosensitive retinal ganglion cells in mice

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