Afferents and Homotypic Neighbors Regulate Horizontal Cell Morphology, Connectivity, and Retinal Coverage

Reese, Benjamin E.; Raven, Mary A.; Stagg, Stephanie B.

doi:10.1523/jneurosci.4876-04.2005

Cited by 76 publications

(118 citation statements)

References 46 publications

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“…Thus, the differences seen here probably arise from differences in connectivity between photoreceptors and horizontal cells, rather than from differences in photoreceptor sensitivity. C57BL/6 horizontal cells have larger dendritic fields than those in 129/Sv retinas (Reese et al, 2005), suggesting that they may contact more cones; this could result in a larger suppression of rod inputs than in 129/Sv retinas.…”

Section: Methodological Considerationsmentioning

confidence: 98%

Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

Trümpler¹,

Dedek²,

Schubert³

et al. 2008

Journal of Neuroscience

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Mammalian B-type horizontal cells make contact with both photoreceptor types: the dendrites contact cone photoreceptors, whereas the axon terminal processes contact rods. Despite their distinct synaptic contacts, horizontal cell somata and axon terminals receive a mixture of rod and cone inputs. Interaction of the two photoreceptor systems is essential for adaptation of photoreceptor sensitivity to different levels of background illumination, and horizontal cells play a key role in this adaptation. In this study, we used transgenic mouse lines to examine the contributions of rod and cone photoreceptor inputs to horizontal cell light responses in the mouse retina: rod signals were isolated by recording intracellularly from horizontal cells in a mouse lacking the cone cyclic nucleotide-gated channel, which lacks cone function, and cone signals were assessed using the rhodopsin knock-out mouse, which is a model for pure cone function. We found that both horizontal cell compartments receive a mixture of inputs from both photoreceptor types. To determine whether these inputs arrive via the long axon connecting the compartments or by way of rod-cone gap junctional coupling, we assessed the rod and cone contributions to horizontal cell somatic and axon terminal light responses in the connexin36-deficient mouse retina, which lacks rodcone coupling. Our results confirm that rods and cones are coupled by connexin36, and suggest that signal transmission along the axon is unidirectional: signals are passed from horizontal cell soma to axon terminal but not from axon terminal to soma.

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Section: Methodological Considerationsmentioning

confidence: 98%

Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

Trümpler¹,

Dedek²,

Schubert³

et al. 2008

Journal of Neuroscience

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“…In these retinae, regular cellular spacing is disrupted when the interference occurs during a critical developmental window during which mosaic regularity is known to increase (Raven et al, 2005a). Furthermore, recent studies that have analyzed the HC mosaic in different strains of mice with a 2-fold difference in total HC number, or in mice with a genetically engineered reduction in normal HC number, have shown that the dendritic area of HCs varies inversely with HC density (Reese et al, 2005;Poché et al, 2008). From these data, it was concluded that mouse HCs employ homotypic cues to restrict dendritic growth, but how such dendritic interactions might mediate intercellular spacing remained unclear.…”

Section: Hcs Employ a Novel Methods Of Mosaic Formationmentioning

confidence: 99%

“…One other unresolved question stemmed from the fact that mature mouse HC dendritic arbors exhibit extensive overlap with neighboring cells (Fig. 4B-D) (Reese et al, 2005). Thus, it remained difficult to envisage how such homotypic signaling might be propagated through dendro-dendritic contacts, assuming that they interact with one another at the tips of their dendrites.…”

Section: Hcs Employ a Novel Methods Of Mosaic Formationmentioning

confidence: 99%

“…One possibility is that such HC mitosis promotes a more efficient laminar coverage of the retina within these species. Should it occur within the mouse retina, however, this explanation would then appear to be at odds with the fact that different strains of mice have HC populations that exhibit conspicuous variations in their total number, and that in the presence of such natural variation (Reese et al, 2005) or following genetic manipulations in mice that yield reduced densities of HCs (Poché et al, 2008), the dendritic fields of HCs modulate their field areas to maintain a constant dendritic coverage. Indeed, this plastic feature of the HC -not witnessed within what is probably the best-studied retinal amacrine cell type with extensive laterally oriented processes, the starburst (cholinergic) amacrine cell (Farajian et al, 2004;Keeley et al, 2007) -is assumed to ensure efficient laminar coverage across the retina.…”

Section: Reviewmentioning

confidence: 99%

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Retinal horizontal cells: challenging paradigms of neural development and cancer biology

Poché

Reese

2009

Development

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A group of retinal interneurons known as horizontal cells has recently been shown to exhibit a variety of unique biological properties, as compared with other nerve cells, that challenge many long-standing assumptions in the fields of neural development and cancer biology. These features include their unusual migratory behavior, their unique morphological plasticity, and their propensity to divide at a relatively late stage during development. Here, we review these novel features, discuss their relevance for other cell types, outline open questions in our understanding of horizontal cell development and consider their implications. IntroductionThe retina, a highly specialized extension of the brain, plays host to the first stages of visual perception. Visual stimuli from the world around us are projected upon the retina, converted into neural signals and transmitted to higher visual centers of the brain via the optic nerve. Despite this complex physiological function, the retina, which is composed of only seven cell types and resides as a thin neuronal sheet in the back of eye, is a deceptively simple structure (Box 1). By studying how the retina develops, we can gain a more thorough understanding of its mature architecture and circuitry and of how these underlie the mechanisms of visual perception, but also come to appreciate the defects in this developmental program that arise as a consequence of genetic mutations that lead to retinal disease.More generally, the retina can be thought of as a 'stripped down' version of the brain, and for this reason it is often utilized as a model system to elucidate fundamental questions regarding the central nervous system (CNS) at large. In terms of neurodevelopment, the retina is a particularly attractive model. Developmental mechanisms that result in a highly specialized and intricately organized neuronal structure composed of precise numbers and ratios of cell types, such as the retina, are very likely to be conserved in other neural contexts. The elucidation of the developmental pathways that function in the retina therefore holds much promise for ultimately understanding some of the mysteries of the brain. Furthermore, owing to it being a non-essential tissue, the retina is an ideal system in which to perform genetic loss-of-function studies, which facilitates a decoding of the genomic control of neurodevelopment. In this review, we focus specifically on new and exciting results pertaining to the development of one type of retinal neuron, the horizontal cell.Retinal horizontal cells (HCs), which were initially characterized by Cajal in 1893 (Cajal, 1893), are, together with amacrine cells, retinal interneurons that lie within the inner nuclear layer (INL) (Fig. 1). HCs function in modulating signaling between photoreceptors and bipolar cells (Box 1). HCs, like all other retinal cell types, are derived from a common retinal progenitor cell population (Turner et al., 1990;Wetts and Fraser, 1988). According to the generally accepted view, these retinal progenitor cells tr...

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“…This large variation across mouse strains is present from the outset of retinal development (11) and is independent of variation in retinal area (9). Furthermore, these horizontal cells modulate their dendritic growth in relation to this variation in cellular density (12), indicating that the determinants of retinal nerve cell number also indirectly impact differentiation.…”

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confidence: 97%

Genetic modulation of horizontal cell number in the mouse retina

Whitney

Raven

Ciobanu

et al. 2011

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

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Neuronal populations display conspicuous variability in their size among individuals, but the genetic sources of this variation are largely undefined. We demonstrate a large and highly heritable variation in neuron number within the mouse retina, affecting a critical population of interneurons, the horizontal cells. Variation in the size of this population maps to the distal end of chromosome (Chr) 13, a region homologous to human Chr 5q11.1–11.2. This region contains two genes known to modulate retinal cell number. Using conditional knock-out mice, we demonstrate that one of these genes, the LIM homeodomain gene Islet-1 ( Isl1 ), plays a role in regulating horizontal cell number. Genetic differences in Isl1 expression are high during the period of horizontal cell production, and cis -regulation of Isl1 expression within the retina is demonstrated directly. We identify a single nucleotide polymorphism in the 5′ UTR of Isl1 that creates an E-box sequence as a candidate causal variant contributing to this variation in horizontal cell number.

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Afferents and Homotypic Neighbors Regulate Horizontal Cell Morphology, Connectivity, and Retinal Coverage

Cited by 76 publications

References 46 publications

Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

Retinal horizontal cells: challenging paradigms of neural development and cancer biology

Genetic modulation of horizontal cell number in the mouse retina

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