Mechanics regulate the postembryonic developmental maturation and function of sensory neurons in a pre-vertebrate chordate.

Abstract

Physical forces are emerging as important contributors to a wide diversity of biological processes across multiple scales and contexts. The development of the nervous system is infuenced by mechanical forces exerted on neurons and glia by the surrounding environment. However, the extent to which tissue mechanics influence the function and morphology of the post-embryonic nervous system remains unclear. Here we leverage the post-embryonic larval period of the pre-vertebrate chordate Ciona intestinalis to study the dynamic interplay between nervous system mechanics, cellular and nuclear morphology and neuronal function. During this post-embryonic period the larval head undergoes substantial stretching along the anterior-posterior axis. We show that this macroscopic morphological change is associated with a significant change in cell and nuclear shape (stretching) of the polymodal sensory neurons located in the papillar organs. Using FRET based genetically encoded tension sensors we show that mechanical tension at the focal adhesions and the nuclear envelope of these papillar sensory neurons increases with time. At the functional level Ca2+ imaging experiments reveal that presentation and removal of a chemosensory stimulus that promotes settlement and metamorphosis elicits significantly stronger responses in late swimming larvae papillar neurons compared to those newly hatched ones. Finally, by combining optoGEF-RhoA dependent control of cellular forces and Ca2+ imaging we demonstrate that the strength of chemosensory responses and settlement behavior can be modulated by mechanical forces.