Presynaptic partner selection during retinal circuit reassembly varies with timing of neuronal regeneration in vivo

Yoshimatsu, Takeshi; D’Orazi, Florence D.; Gamlin, Clare; Suzuki, Sachihiro C.; Suli, Arminda; Kimelman, David; Raible, David W.; Wong, Rachel

doi:10.1038/ncomms10590

Cited by 60 publications

(89 citation statements)

References 50 publications

(62 reference statements)

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“…Our current study shows that replacement neurons are able to form synapses with mature circuitry, an observation previously made in other CNS systems after damage [24–26, 30, 32, 33, 40–44]. Further, we found that although regenerated xfz43 BCs establish their original numbers of input synapses, the axons of all three BC types doubled their number of ribbons.…”

Section: Discussionsupporting

confidence: 87%

“…To visualize individual BCs, we injected pUAS:MYFP or pUAS:MmTFP1myc [44] into single-cell stage embryos from the xfz43 line. To track the same retinal areas across ages for live-imaging, we injected pCrx:MYFP [39] into single-cell embryos from xfz43 fish crossed with the Vsx1 line (see Supplemental Experimental Procedures).…”

Section: Methodsmentioning

confidence: 99%

“…Mitotic cells were labeled in live larvae by immersion in a solution containing 0.5 mM F-ara-EdU [44] (Sigma T511293) in system water. The duration of treatment was timed according to the experimental paradigm.…”

Section: Methodsmentioning

confidence: 99%

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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: Discussionsupporting

confidence: 87%

Section: Methodsmentioning

confidence: 99%

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

et al. 2016

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“…Other work suggests that the formation of functional synapses after input loss is possible. For example, recent work in the zebrafish retina suggests that, after postsynaptic neurons are killed, newly born neurons can form synapses with the presynaptic partners but only during a limited time window (Yoshimatsu et al 2016). More systems to study dendrite regeneration will be required to address whether dendrites regenerated by injured, but not killed, neurons can form functional synapses.…”

Section: Comparison With Other Studies Of Dendrite Regenerationmentioning

confidence: 99%

In vivo dendrite regeneration after injury is different from dendrite development

Thompson-Peer

DeVault

et al. 2016

Genes Dev.

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Neurons receive information along dendrites and send signals along axons to synaptic contacts. The factors that control axon regeneration have been examined in many systems, but dendrite regeneration has been largely unexplored. Here we report that, in intact Drosophila larvae, a discrete injury that removes all dendrites induces robust dendritic growth that recreates many features of uninjured dendrites, including the number of dendrite branches that regenerate and responsiveness to sensory stimuli. However, the growth and patterning of injury-induced dendrites is significantly different from uninjured dendrites. We found that regenerated arbors cover much less territory than uninjured neurons, fail to avoid crossing over other branches from the same neuron, respond less strongly to mechanical stimuli, and are pruned precociously. Finally, silencing the electrical activity of the neurons specifically blocks injury-induced, but not developmental, dendrite growth. By elucidating the essential features of dendrites grown in response to acute injury, our work builds a framework for exploring dendrite regeneration in physiological and pathological conditions.

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“…Proliferative cells show a bias towards generating ablated cell fates, but also generate non-ablated cells [33, 35, 36]. This shows their intrinsic multipotency and may reflect recapitulation of intrinsic molecular processes that control temporal cell fate decision as observed in development.…”

Section: Introductionmentioning

confidence: 99%

Fate bias during neural regeneration adjusts dynamically without recapitulating developmental fate progression

2017

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BackgroundRegeneration of neurons in the central nervous system is poor in humans. In other vertebrates neural regeneration does occur efficiently and involves reactivation of developmental processes. Within the neural retina of zebrafish, Müller glia are the main stem cell source and are capable of generating progenitors to replace lost neurons after injury. However, it remains largely unknown to what extent Müller glia and neuron differentiation mirror development.MethodsFollowing neural ablation in the zebrafish retina, dividing cells were tracked using a prolonged labelling technique. We investigated to what extent extrinsic feedback influences fate choices in two injury models, and whether fate specification follows the histogenic order observed in development.ResultsBy comparing two injury paradigms that affect different subpopulations of neurons, we found a dynamic adaptability of fate choices during regeneration. Both injuries followed a similar time course of cell death, and activated Müller glia proliferation. However, these newly generated cells were initially biased towards replacing specifically the ablated cell types, and subsequently generating all cell types as the appropriate neuron proportions became re-established. This dynamic behaviour has implications for shaping regenerative processes and ensuring restoration of appropriate proportions of neuron types regardless of injury or cell type lost.ConclusionsOur findings suggest that regenerative fate processes are more flexible than development processes. Compared to development fate specification we observed a disruption in stereotypical birth order of neurons during regeneration Understanding such feedback systems can allow us to direct regenerative fate specification in injury and diseases to regenerate specific neuron types in vivo.

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Presynaptic partner selection during retinal circuit reassembly varies with timing of neuronal regeneration in vivo

Cited by 60 publications

References 50 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

In vivo dendrite regeneration after injury is different from dendrite development

Fate bias during neural regeneration adjusts dynamically without recapitulating developmental fate progression

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