Abstract
BackgroundMany neurons in the central nervous system, including retinal ganglion cells (RGCs), possess asymmetric dendritic arbors oriented toward their presynaptic partners. How such dendritic arbors become biased during development in vivo is not well understood. Dendritic arbors may become oriented by directed outgrowth or by reorganization of an initially unbiased arbor. To distinguish between these possibilities, we imaged the dynamic behavior of zebrafish RGC dendrites during development in vivo. We then addressed how cell positioning within the retina, altered in heart-and-soul (has) mutants, affects RGC dendritic orientation.ResultsIn vivo multiphoton time-lapse analysis revealed that RGC dendrites initially exhibit exploratory behavior in multiple directions but progressively become apically oriented. The lifetimes of basal and apical dendrites were generally comparable before and during the period when arbors became biased. However, with maturation, the addition and extension rates of basal dendrites were slower than those of the apical dendrites. Oriented dendritic arbors were also found in misplaced RGCs of the has retina but there was no preferred orientation amongst the population. However, has RGCs always projected dendrites toward nearby neuropil where amacrine and bipolar cell neurites also terminated. Chimera analysis showed that the abnormal dendritic organization of RGCs in the mutant was non-cell autonomous.ConclusionsOur observations show that RGC dendritic arbors acquire an apical orientation by selective and gradual restriction of dendrite addition to the apical side of the cell body, rather than by preferential dendrite stabilization or elimination. A biased arbor emerges at a stage when many of the dendritic processes still appear exploratory. The generation of an oriented RGC dendritic arbor is likely to be determined by cell-extrinsic cues. Such cues are unlikely to be localized to the basal lamina of the inner retina, but rather may be provided by cells presynaptic to the RGCs.
Highlights
Many neurons in the central nervous system, including retinal ganglion cells (RGCs), possess asymmetric dendritic arbors oriented toward their presynaptic partners
By examining RGC dendritic morphology at various stages, we found that most RGCs initiate dendritic development between 36 and 60 hpf, cell division and differentiation were still occurring at 60 hpf at the front of the developmental wave in peripheral retina
To determine how dendritic orientation is established with cellular maturation, we compared RGCs in relatively immature regions to those from more mature regions within or across animals
Summary
Many neurons in the central nervous system, including retinal ganglion cells (RGCs), possess asymmetric dendritic arbors oriented toward their presynaptic partners. Many neurons in the central nervous system, including Purkinje cells [2], retinal ganglion cells (RGCs) [3,4], layer IV neurons of the somatosensory cortex [5,6], mitral cells in the rodent olfactory bulb [7,8,9,10] and projection neurons in the fly olfactory system [11,12], form asymmetric dendritic arbors that are directed toward their presynaptic partners Such asymmetric shapes of dendritic trees facilitate investigations into the cellular mechanisms that. Classic examples of neurons adopting this strategy are Purkinje cells [2,18] and spiny stellate cells of the barrel cortex [5,6]
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