Direction selectivity in the retina: symmetry and asymmetry in structure and function

Vaney, David I.; Sivyer, Benjamin; Taylor, W. Rowland

doi:10.1038/nrn3165

Cited by 290 publications

(323 citation statements)

References 130 publications

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“…Physiological studies have revealed the existence of four ooDSGC subsets, responsive to upward, downward, nasal, and temporal motion (31). These subsets are morphologically similar but molecularly distinct: cdh6 is expressed primarily by ooDSGCs selective for vertical motion, whereas ooDSGCs sensitive to temporal motion express MMP17 (22).…”

Section: Resultsmentioning

confidence: 99%

Direction-selective retinal ganglion cells arise from molecularly specified multipotential progenitors

Huerta

Kim

Voinescu

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Single progenitors can give rise to any and all of the main retinal cell types: photoreceptors, interneurons (horizontal, bipolar, and amacrine cells), retinal ganglion cells (RGCs), and glia. Many of these types are divisible into multiple functionally, structurally, and molecularly distinct subtypes (e.g., ∼25 for RGCs). It remains unknown when and how progenitors become committed to generate such subtypes. Here, we determine the origin of RGCs that respond selectively to vertical motion and express cadherin 6 (cdh6). Using Cre recombinase-based lineage tracing, we show that these RGCs arise from progenitors that themselves express cdh6. These progenitors are capable of generating all major retinal cell types, but the RGCs they generate are predominantly of the single direction-selective subtype. In contrast, cdh6-positive progenitors retain the ability to generate multiple subtypes of amacrine and bipolar cells. Our results demonstrate that type and subtype specification are regulated in different ways and suggest that multipotential but fate-restricted progenitors contribute to subtype specification in retina.

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Section: Resultsmentioning

confidence: 99%

Direction-selective retinal ganglion cells arise from molecularly specified multipotential progenitors

Huerta

Kim

Voinescu

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…These are distinguishable from On-DSGCs in several ways: (1) their dendrites are bistratified rather than monostratified; (2) they respond to both light increments and decrements; (3) they prefer higher velocity visual stimuli; and (4) on average they have smaller dendritic and receptive fields than On-DSGCs (Barlow and Hill, 1963;Barlow and Hill, 1964;Weng et al, 2005;Rivlin-Etzion et al, 2011). On-Off DSGCs encode direction along one of the four cardinal axes: (1) upward; (2) downward; (3) forward; or (4) backward (Borst and Euler, 2011;Vaney et al, 2012). In both rabbits and mice, On-Off DSGCs project to the dorsal lateral geniculate nucleus (dLGN) and superior colliculus (SC), visual targets associated with spatial vision and reorientation of gaze, respectively (Pu and Amthor, 1990;Huberman et al, 2009;Kay et al, 2011;Rivlin-Etzion et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Genetic Dissection of Retinal Inputs to Brainstem Nuclei Controlling Image Stabilization

et al. 2013

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When the head rotates, the image of the visual world slips across the retina. A dedicated set of retinal ganglion cells (RGCs) and brainstem visual nuclei termed the "accessory optic system" (AOS) generate slip-compensating eye movements that stabilize visual images on the retina and improve visual performance. Which types of RGCs project to each of the various AOS nuclei remain unresolved. Here we report a new transgenic mouse line, Hoxd10 -GFP, in which the RGCs projecting to all the AOS nuclei are fluorescently labeled. Electrophysiological recordings of Hoxd10 -GFP RGCs revealed that they include all three subtypes of On direction-selective RGCs (On-DSGCs), responding to upward, downward, or forward motion. Hoxd10 -GFP RGCs also include one subtype of On-Off DSGCs tuned for forward motion. Retrograde circuit mapping with modified rabies viruses revealed that the On-DSGCs project to the brainstem centers involved in both horizontal and vertical retinal slip compensation. In contrast, the On-Off DSGCs labeled in Hoxd10 -GFP mice projected to AOS nuclei controlling horizontal but not vertical image stabilization. Moreover, the forward tuned On-Off DSGCs appear physiologically and molecularly distinct from all previously genetically identified On-Off DSGCs. These data begin to clarify the cell types and circuits underlying image stabilization during self-motion, and they support an unexpected diversity of DSGC subtypes.

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“…Combined with the centrifugal tuning of SACs (Euler et al 2002), this asymmetric wiring should, in theory, be sufficient to confer direction selectivity on the RGC ( Fig. 7C; Demb 2007;Vaney et al 2012). Rather, asymmetric wiring from SACs alone is sufficient to generate direction-selective responses in both ON DSGCs and ON-OFF direction-selective ganglion cells (Yonehara et al 2013;Park et al 2014).…”

Section: Visualizing the Functional Properties Of Identified Drosophimentioning

confidence: 99%

So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice

2014

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The visual system is a powerful model for probing the development, connectivity, and function of neural circuits. Two genetically tractable species, mice and flies, are together providing a great deal of understanding of these processes. Current efforts focus on integrating knowledge gained from three cross-fostering fields of research: (1) understanding how the fates of different cell types are specified during development, (2) revealing the synaptic connections between identified cell types (''connectomics'') by high-resolution three-dimensional circuit anatomy, and (3) causal testing of how identified circuit elements contribute to visual perception and behavior. Here we discuss representative examples from fly and mouse models to illustrate the ongoing success of this tripartite strategy, focusing on the ways it is enhancing our understanding of visual processing and other sensory systems.For many decades, the visual systems of both vertebrates and invertebrates have been a favorite arena for understanding how neural circuits are built and function. A considerable body of work has focused on the specification of cell types of the retina; for instance, the designation of different classes of photoreceptors with distinct spectral sensitivities in the Drosophila retina (Rister and Desplan 2011) and the establishment of the various cell types that comprise the vertebrate retina: photoreceptors, Muller glia, interneurons (horizontal, amacrine, and bipolar cells), and retinal ganglion cells (RGCs) (Livesey and Cepko 2001;Mu et al. 2004;Poch e and Reese 2006). With that knowledge in hand, focus in recent years has expanded to understanding how the circuits formed by these retinal cells are linked to the staggering number of diverse visual neurons in the brain, which in turn enables sophisticated and diverse computational tasks. The ultimate goal is to understand how cellular identity, function, and connectivity relate to visually guided behaviors. (Fig. 1A).

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Direction selectivity in the retina: symmetry and asymmetry in structure and function

Cited by 290 publications

References 130 publications

Direction-selective retinal ganglion cells arise from molecularly specified multipotential progenitors

Direction-selective retinal ganglion cells arise from molecularly specified multipotential progenitors

Genetic Dissection of Retinal Inputs to Brainstem Nuclei Controlling Image Stabilization

So many pieces, one puzzle: cell type specification and visual circuitry in flies and mice

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