Abstract
BackgroundNeuronal connections are often arranged in layers, which are divided into sublaminae harboring synapses with similar response properties. It is still debated how fine-grained synaptic layering is established during development. Here we investigated two stratified areas of the zebrafish visual pathway, the inner plexiform layer (IPL) of the retina and the neuropil of the optic tectum, and determined if activity is required for their organization.ResultsThe IPL of 5-day-old zebrafish larvae is composed of at least nine sublaminae, comprising the connections between different types of amacrine, bipolar, and ganglion cells (ACs, BCs, GCs). These sublaminae were distinguished by their expression of cell type-specific transgenic fluorescent reporters and immunohistochemical markers, including protein kinase Cβ (PKC), parvalbumin (Parv), zrf3, and choline acetyltransferase (ChAT). In the tectum, four retinal input layers abut a laminated array of neurites of tectal cells, which differentially express PKC and Parv. We investigated whether these patterns were affected by experimental disruptions of retinal activity in developing fish. Neither elimination of light inputs by dark rearing, nor a D, L-amino-phosphono-butyrate-induced reduction in the retinal response to light onset (but not offset) altered IPL or tectal lamination. Moreover, thorough elimination of chemical synaptic transmission with Botulinum toxin B left laminar synaptic arrays intact.ConclusionOur results call into question a role for activity-dependent mechanisms – instructive light signals, balanced on and off BC activity, Hebbian plasticity, or a permissive role for synaptic transmission – in the synaptic stratification we examined. We propose that genetically encoded cues are sufficient to target groups of neurites to synaptic layers in this vertebrate visual system.
Highlights
Neuronal connections are often arranged in layers, which are divided into sublaminae harboring synapses with similar response properties
A small population of interplexiform cells in the inner nuclear layer (INL) are labeled with tyrosine hydroxylase (TH) antisera [23] (Additional file 1)
Our study suggests that the established roles of synaptic transmission in mammalian visual pathway refinement are particular to that lineage; an organized inner plexiform layer (IPL) and tectal neuropil can be assembled by hardwiring mechanisms alone
Summary
Neuronal connections are often arranged in layers, which are divided into sublaminae harboring synapses with similar response properties. It is still debated how fine-grained synaptic layering is established during development. The formation of neuronal connections is commonly thought to occur in two stages. Genetically encoded processes, such as axon guidance by molecular cues, establish coarse connectivity by bringing presynaptic and postsynaptic partners in spatial proximity. Electrical activity is said to serve in selecting synaptic partners. According to Hebb's principle, connections between neurons with temporally correlated activity patterns are strengthened, whereas synapses between neurons with divergent activation patterns are eliminated. Correlated activity could, in principle, originate either from sensory experience or from patterns of (page number not for citation purposes)
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