Clonal Relationships Impact Neuronal Tuning within a Phylogenetically Ancient Vertebrate Brain Structure

Understanding 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.