Multivariate analysis of electrophysiological diversity of Xenopus visual neurons during development and plasticity

Abstract

Biophysical properties of neurons become increasingly diverse over development, but mechanisms underlying and constraining this diversity are not fully understood. Here we investigate electrophysiological characteristics of Xenopus tadpole midbrain neurons across development and during homeostatic plasticity induced by patterned visual stimulation. We show that in development tectal neuron properties not only change on average, but also become increasingly diverse. After sensory stimulation, both electrophysiological diversity and functional differentiation of cells are reduced. At the same time, the amount of cross-correlations between cell properties increase after patterned stimulation as a result of homeostatic plasticity. We show that tectal neurons with similar spiking profiles often have strikingly different electrophysiological properties, and demonstrate that changes in intrinsic excitability during development and in response to sensory stimulation are mediated by different underlying mechanisms. Overall, this analysis and the accompanying dataset provide a unique framework for further studies of network maturation in Xenopus tadpoles.

DOI: http://dx.doi.org/10.7554/eLife.11351.001

eLife digest

Brains consist of many cells called neurons: billions of them in a human brain, and hundreds of thousands in the brain of a small fish or a frog tadpole. Many of these neurons are very much alike, and work together to process information in the brain. Yet while they are similar, they are not exactly identical. One of the reasons for these differences seems to be to allow each neuron to contribute something unique to the overall working of the brain. By looking at how individual neurons within a specific type differ from each other, it is possible to understand more about how they work together.

Ciarleglio, Khakhalin et al. have now compared the properties of the neurons in a part of the brain of a developing frog tadpole that processes sensory information. This showed that these neurons appear relatively similar to each other in young tadpoles. However, as the tadpoles grow and their brains become more elaborate the neurons become increasingly diverse, and their properties become more unique and nuanced.

One possible explanation is that this diversity reflects new types of neurons being formed; another, that the differences between the neurons reflect how these cells have adapted to different patterns of sensory input they may have experienced. To distinguish between these two possibilities, Ciarleglio, Khakhalin et al. provided a group of older tadpoles with strobe-like visual stimulation and observed that this caused the neurons to become more similar once again. This suggests that neurons can change their response properties to adapt to the type of sensory input they receive, which would allow the animal to better process different types of sensory information. The data collected through these experiments could now be used to build computational models of this part of the tadpole brain.

DOI: http://dx.doi.org/10.7554/eLife.11351.002