Shear forces drive precise patterning of hair cells in the mammalian inner ear

Roie Cohen ^1,2 Liat Amir-Zilberstein ¹ Micha Hersch ^3,4 Shiran Wolland ¹ Shahar Taiber ^1,5 Fumio Matsuzaki ⁶ Svenn Bergmann ^3,4,7 Karen Avraham ⁵ David Sprinzak ¹

¹School of Neurobiology, Biochemistry and Biophysics, George S. Wise Faculty of Life Sciences, Tel-Aviv University, Israel
²Raymond and Beverly Sackler School of Physics and Astronomy, Faculty of Exact Sciences, Tel-Aviv University, Israel
³Department of Computational Biology, University of Lausanne, Switzerland
⁴Department of Bioinformatics, Swiss Institute of Bioinformatics, Switzerland
⁵Department of Human Molecular Genetics and Biochemistry, Sackler Faculty of Medicine and Sagol School of Neuroscience, Tel-Aviv University, Israel
⁶Laboratory of Cell Asymmetry, Riken Center for Biosystems Dynamics Research, Japan
⁷Department of Integrative Biomedical Sciences, University of Cape Town, South Africa

The mammalian hearing organ, the organ of Corti, consists of a precisely organized checkerboard-like pattern of four rows of hair cells (HCs) interspersed by non-sensory supporting cells (SCs). How such precise patterning emerges during development is not well understood. Using a combination of quantitative morphological analysis and time-lapse imaging of mouse cochlear explants, we show that patterning of the organ of Corti involves dynamic reorganizations that include lateral shear motion, cell intercalations, and delaminations. A mathematical model, where tissue morphology is described in terms of the mechanical forces that act on cells and cellular junctions, suggests that global shear on HCs and local repulsion between HCs are sufficient to drive the tissue into the final checkerboard-like pattern. Our findings suggest that precise patterns can emerge during development from reorganization processes, driven by a combination of global and local forces in a process analogous to shear-induced crystallization in physics