The distribution of the preferred directions of the ON-OFF direction selective ganglion cells in the rabbit retina requires refinement after eye opening

Chan, Yu-Chen; Chiao, Chuan-Chin

doi:10.1002/phy2.13

Cited by 15 publications

(20 citation statements)

References 67 publications

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“…A recent study demonstrated that at eye-opening in both rabbit and mouse, the distribution of preferred directions was uniformly distributed, rather than showing segregation along the four cardinal axes, indicating that a process of refinement in the preferred direction occurs after eye-opening (Chan & Chiao, 2013). They also found a slight degree of anisotropy in the distribution of preferred directions in dark reared animals.…”

Section: Discussionmentioning

confidence: 99%

“…The development of direction selective circuits does not require visual experience because direction selectivity is already established at eye opening (Elstrott et al , 2008; Chan & Chiao, 2008; Chen et al , 2009; Wei et al , 2011; Chen et al , 2014), though several features of DSGCs are immature at these early ages (Chan & Chiao, 2008, 2013; Chen et al , 2014). However, spontaneous activity may play a role.…”

Section: Introductionmentioning

confidence: 99%

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CaV3.2 KO mice have altered retinal waves but normal direction selectivity

et al. 2015

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Early in development, before the onset of vision, the retina establishes direction-selective responses. During this time period, the retina spontaneously generates bursts of action potentials that propagate across its extent. The precise spatial and temporal properties of these “retinal waves” have been implicated in the formation of retinal projections to the brain. However their role in the development of direction selective circuits within the retina has not yet been determined. We addressed this issue by combining multi-electrode array and cell-attached recordings to examine mice that lack the CaV3.2 subunit of T-type Ca2+ channels (CaV3.2 KO) because these mice exhibit disrupted waves during the period that direction selective circuits are established. We found that the spontaneous activity of these mice displays wave-associated bursts of action potentials that are altered from control mice: the frequency of these bursts is significantly decreased and the firing rate within each burst is reduced. Moreover, the retina’s projection patterns demonstrate decreased eye-specific segregation in the dLGN. However, after eye-opening, the direction selective responses of CaV3.2 KO DSGCs are indistinguishable from those of wild-type DSGCs. Our data indicate that, although the temporal properties of the action potential bursts associated with retinal waves are important for activity-dependent refining of retinal projections to central targets, they are not critical for establishing direction selectivity in the retina.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

CaV3.2 KO mice have altered retinal waves but normal direction selectivity

et al. 2015

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“…To compare the extent of clustering, we computed the silhouette value, with higher silhouette values indicating an appropriate number of clusters [20,21] (see Supplemental Information). Adult retinas displayed significantly higher silhouette values for 3 and 4 specific clusters for the ON and the ON-OFF DSGCs, respectively than a random distribution of preferred directions (0.91 and 0.89).…”

Section: Clustering Of Dsgc Preferred Directions Along Cardinal Axes mentioning

confidence: 99%

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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“…They comprise four subtypes, each preferring one of four cardinal directions 16–18 . The polar distribution of directional preferences among ON‐OFF‐DSGCs appears cruciform, with four lobes separated by 90° (Fig.…”

Section: Introductionmentioning

confidence: 99%

A retinal code for motion along the gravitational and body axes

Sabbah

Gemmer

Bhatia-Lin

et al. 2017

Nature

140

172

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Summary Self-motion triggers complementary visual and vestibular reflexes supporting image-stabilization and balance. Translation through space produces one global pattern of retinal image motion (optic flow), rotation another. We show that each subtype of direction-selective ganglion cell (DSGC) adjusts its direction preference topographically to align with specific translatory optic flow fields, creating a neural ensemble tuned for a specific direction of motion through space. Four cardinal translatory directions are represented, aligned with two axes of high adaptive relevance: the body and gravitational axes. One subtype maximizes its output when the mouse advances, others when it retreats, rises, or falls. ON-DSGCs and ON-OFF-DSGCs share the same spatial geometry but weight the four channels differently. Each subtype ensemble is also tuned for rotation. The relative activation of DSGC channels uniquely encodes every translation and rotation. Though retinal and vestibular systems both encode translatory and rotatory self-motion, their coordinate systems differ.

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The distribution of the preferred directions of the ON-OFF direction selective ganglion cells in the rabbit retina requires refinement after eye opening

Cited by 15 publications

References 67 publications

CaV3.2 KO mice have altered retinal waves but normal direction selectivity

CaV3.2 KO mice have altered retinal waves but normal direction selectivity

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

A retinal code for motion along the gravitational and body axes

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