Neuronal remodeling in retinal circuit assembly, disassembly, and reassembly

D’Orazi, Florence D.; Suzuki, Sachihiro C.; Wong, Rachel

doi:10.1016/j.tins.2014.07.009

Cited by 51 publications

(45 citation statements)

References 105 publications

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“…How do xfz43 BCs bias their synaptic connectivity towards a single or subset of cone types? A common developmental mechanism that shapes to the stereotypic wiring of a neuron is the elimination of surplus synapses, or of contacts with inappropriate partner types [36, 37]. This does not appear to occur for xfz43 BCs, which showed no loss of synapses with any partner type over time, but instead preferentially increased synaptogenesis with their primary synaptic partner(s).…”

Section: Discussionmentioning

confidence: 99%

Mismatch of Synaptic Patterns between Neurons Produced in Regeneration and during Development of the Vertebrate Retina

et al. 2016

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Summary Stereotypic patterns of synaptic connections between neurons underlie the ability of the central nervous system (CNS) to perform complex but circuit-specific information processing. Tremendous progress has been made toward advancing our understanding of how circuits are assembled during development, but whether the precision of this process can be recaptured after regeneration of neurons in the damaged CNS remains unclear. Here, we harnessed the endogenous regenerative capacity of the zebrafish retina to reconstruct the circuitry of neurons produced after damage. We tracked the input connectivity of identified bipolar cell (BC) types across stages of retinal development, and after BC regeneration. We found that BCs of each type generate a unique and stereotypic wiring pattern with cone photoreceptors by gaining synapses with specific photoreceptor types over time. After selective ablation, the targeted BC types are rapidly reproduced and largely re-establish their characteristic morphological features. The regenerated population connects with appropriate photoreceptor types and establishes the original number of synaptic contacts. However, BC types that normally bias their connectivity in favor of red cones fail to precisely recapture this synaptic partner preference upon regeneration. Furthermore, regenerated BCs succeed in forming synaptic specializations at their axon terminals, but in excess of the usual number. Altogether, we find that regenerated BCs reinstate some, but not all major features of their stereotypic wiring, suggesting that circuit patterns may be unable to regenerate with the same fidelity as in development.

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Section: Discussionmentioning

confidence: 99%

Mismatch of Synaptic Patterns between Neurons Produced in Regeneration and during Development of the Vertebrate Retina

et al. 2016

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“…We show that deafferented S-cone bipolar cells effectively expand their dendritic field by creating new dendritic branches, which elongate and explore within the OPL until encountering an S-cone and creating a new synapse. Likewise, strategies for dendritic expansion during normal development are known to include the creation of new dendritic branches, as well as dendritic elongation [4,31,32]. However, developmental dendritic expansion strategies are known to differ even amongst bipolar cell types [33].…”

Section: Discussionmentioning

confidence: 99%

Stereotyped Synaptic Connectivity Is Restored during Circuit Repair in the Adult Mammalian Retina

2018

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Proper function of the central nervous system (CNS) depends on the specificity of synaptic connections between cells of various types. Cellular and molecular mechanisms responsible for the establishment and refinement of these connections during development are the subject of an active area of research [1-6]. However, it is unknown if the adult mammalian CNS can form new type-selective synapses following neural injury or disease. Here, we assess whether selective synaptic connections can be reestablished after circuit disruption in the adult mammalian retina. The stereotyped circuitry at the first synapse in the retina, as well as the relatively short distances new neurites must travel compared to other areas of the CNS, make the retina well suited to probing for synaptic specificity during circuit reassembly. Selective connections between short-wavelength sensitive cone photoreceptors (S-cones) and S-cone bipolar cells provides the foundation of the primordial blue-yellow vision, common to all mammals [7-18]. We take advantage of the ground squirrel retina, which has a one-to-one S-cone-to-S-cone-bipolar-cell connection, to test if this connectivity can be reestablished following local photoreceptor loss [8, 19]. We find that after in vivo selective photoreceptor ablation, deafferented S-cone bipolar cells expand their dendritic trees. The new dendrites randomly explore the proper synaptic layer, bypass medium-wavelength sensitive cone photoreceptors (M-cones), and selectively synapse with S-cones. However, non-connected dendrites are not pruned back to resemble unperturbed S-cone bipolar cells. We show, for the first time, that circuit repair in the adult mammalian retina can recreate stereotypic selective wiring.

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“…Conversely, if only glutamate release from the presynapse is reduced, but the rod itself is maintained, ectopic synapses between rods and rod bipolar cells are formed and mGluR6 distribution is strongly altered (reviewed in ref. 9). In this issue of the JCI, Ou, Vijayasarathy, and colleagues report a subtle pathosynaptic phenotype in a mouse model for XLRS.…”

Section: Murine Xlrs Model Provides Insight Into Pathosynaptic Phenotmentioning

confidence: 99%

Restoration of synaptic function in sight for degenerative retinal disease

Schubert¹,

Wissinger²

2015

J. Clin. Invest.

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Neuronal remodeling in retinal circuit assembly, disassembly, and reassembly

Cited by 51 publications

References 105 publications

Mismatch of Synaptic Patterns between Neurons Produced in Regeneration and during Development of the Vertebrate Retina

Mismatch of Synaptic Patterns between Neurons Produced in Regeneration and during Development of the Vertebrate Retina

Stereotyped Synaptic Connectivity Is Restored during Circuit Repair in the Adult Mammalian Retina

Restoration of synaptic function in sight for degenerative retinal disease

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