In Vivo Study of Dynamics and Stability of Dendritic Spines on Olfactory Bulb Interneurons in Xenopus laevis Tadpoles.

Yu-Bin Huang,Li Zhang,Wu Yin,Bing Hu,Chun-Rui Hu,Xiangming Zha

doi:10.1371/journal.pone.0140752

Yu-Bin Huang, Li Zhang + Show 4 more

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https://doi.org/10.1371/journal.pone.0140752

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Abstract

Dendritic spines undergo continuous remodeling during development of the nervous system. Their stability is essential for maintaining a functional neuronal circuit. Spine dynamics and stability of cortical excitatory pyramidal neurons have been explored extensively in mammalian animal models. However, little is known about spiny interneurons in non-mammalian vertebrate models. In the present study, neuronal morphology was visualized by single-cell electroporation. Spiny neurons were surveyed in the Xenopus tadpole brain and observed to be widely distributed in the olfactory bulb and telencephalon. DsRed- or PSD95-GFP-expressing spiny interneurons in the olfactory bulb were selected for in vivo time-lapse imaging. Dendritic protrusions were classified as filopodia, thin, stubby, or mushroom spines based on morphology. Dendritic spines on the interneurons were highly dynamic, especially the filopodia and thin spines. The stubby and mushroom spines were relatively more stable, although their stability significantly decreased with longer observation intervals. The 4 spine types exhibited diverse preferences during morphological transitions from one spine type to others. Sensory deprivation induced by severing the olfactory nerve to block the input of mitral/tufted cells had no significant effects on interneuron spine stability. Hence, a new model was established in Xenopus laevis tadpoles to explore dendritic spine dynamics in vivo.

Highlights

The dendritic spine, a small membranous protrusion from a neuron’s dendrite, is a postsynaptic structure that stores synaptic strength and transmits electrical signals within neural circuits
Granule cells in the olfactory bulb (OB) of Xenopus are the only reported spiny neurons according to morphology in slices [31, 34]. Is this the only spiny neuron with typical morphology in Xenopus? What are the dynamic features of this model? In this study, we examined the distribution of spiny neurons in the Xenopus brain, as well as dynamic changes and stability of spiny neurons in the OB during development and after odor deprivation
The granule cell is the only reported spiny neuron based on morphology in Xenopus OB slice [31, 34], and little is known about other types of spiny neuron

Summary

Introduction

The dendritic spine, a small membranous protrusion from a neuron’s dendrite, is a postsynaptic structure that stores synaptic strength and transmits electrical signals within neural circuits. To decipher complex brain functions and disorders, non-mammalian vertebrates such as zebrafish and Xenopus offer unique advantages and simplified but significant structural and functional homology to the human central nervous system and have been used to study synaptogenesis and dendrite development [15,16,17,18,19,20,21,22,23,24,25]. Most knowledge about spine morphology and dynamic features has been gained from studies on mammalian brains in barrel, visual, and motor cortices [4, 5, 10, 26]

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