Abstract
SummaryUnderstanding how neurons acquire specific response properties is a major goal in neuroscience. Recent studies in mouse neocortex have shown that “sister neurons” derived from the same cortical progenitor cell have a greater probability of forming synaptic connections with one another [1, 2] and are biased to respond to similar sensory stimuli [3, 4]. However, it is unknown whether such lineage-based rules contribute to functional circuit organization across different species and brain regions [5]. To address this question, we examined the influence of lineage on the response properties of neurons within the optic tectum, a visual brain area found in all vertebrates [6]. Tectal neurons possess well-defined spatial receptive fields (RFs) whose center positions are retinotopically organized [7]. If lineage relationships do not influence the functional properties of tectal neurons, one prediction is that the RF positions of sister neurons should be no more (or less) similar to one another than those of neighboring control neurons. To test this prediction, we developed a protocol to unambiguously identify the daughter neurons derived from single tectal progenitor cells in Xenopus laevis tadpoles. We combined this approach with in vivo two-photon calcium imaging in order to characterize the RF properties of tectal neurons. Our data reveal that the RF centers of sister neurons are significantly more similar than would be expected by chance. Ontogenetic relationships therefore influence the fine-scale topography of the retinotectal map, indicating that lineage relationships may represent a general and evolutionarily conserved principle that contributes to the organization of neural circuits.
Highlights
To examine whether lineage-based rules contribute to functional circuit organization in the optic tectum, we developed a method for labeling a single neuronal clone per animal, which enabled us to definitively identify sister tectal neurons
From a total of 438 animals in which we confirmed that a single progenitor cell was labeled, 103 contained two or more labeled sister neurons when the animal was reimaged 6–19 days later at stage 49 or 50 (Figure 1C)
For clones to be included in the analysis, labeled neurons were required to exhibit robust spatially localized receptive fields (RFs), as determined statistically by fitting each RF with a 2D Gaussian function (Figures 3D and 3E; Supplemental Experimental Procedures)
Summary
To examine whether lineage-based rules contribute to functional circuit organization in the optic tectum, we developed a method for labeling a single neuronal clone per animal, which enabled us to definitively identify sister tectal neurons. There was a strong tendency for neurons derived from the same progenitor to be situated within nearby cell-dense layers (p < 2 3 1025, bootstrap test; Figure 2C; Supplemental Experimental Procedures).
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