How the embryonic chick brain twists.
During early development, the tubular embryonic chick brain undergoes a combination of progressive ventral bending and rightward torsion, one of the earliest organ-level left-right asymmetry events in development. Existing evidence suggests that bending is caused by differential growth, but the mechanism for the predominantly rightward torsion of the embryonic brain tube remains poorly understood. Here, we show through a combination ofin vitroexperiments, a physical model of the embryonic morphology and mechanics analysis that the vitelline membrane (VM) exerts an external load on the brain that drives torsion. Our theoretical analysis showed that the force is of the order of 10 micronewtons. We also designed an experiment to use fluid surface tension to replace the mechanical role of the VM, and the estimated magnitude of the force owing to surface tension was shown to be consistent with the above theoretical analysis. We further discovered that the asymmetry of the looping heart determines the chirality of the twisted brain via physical mechanisms, demonstrating the mechanical transfer of left-right asymmetry between organs. Our experiments also implied that brain flexure is a necessary condition for torsion. Our work clarifies the mechanical origin of torsion and the development of left-right asymmetry in the early embryonic brain.
Department of Biomedical Engineering, Washington University, St Louis, MO 63130, USA zi.chen@dartmouth.edu.|Thayer School of Engineering, Dartmouth College, Hanover, NH 03755, USA.
Zi
0000-0001-5927-0249
Z
Chen
School of Materials Science and Engineering, Fujian University of Technology, Fuzhou 350108, People's Republic of China.|Fujian Provincial Key Laboratory of Advanced Materials Processing and Application, Fuzhou 350108, People's Republic of China.
Qiaohang
Q
Guo
Department of Biomedical Engineering, Washington University, St Louis, MO 63130, USA.
Eric
E
Dai
Department of Biomedical Engineering, Washington University, St Louis, MO 63130, USA.|Department of Bioengineering, University of California at San Diego, La Jolla, CA 92093, USA.
Nickolas
N
Forsch
Department of Biomedical Engineering, Washington University, St Louis, MO 63130, USA.
Larry A
LA
Taber
D000818:Animals; D001921:Brain / Q000196:embryology*; D002642:Chick Embryo; D002645:Chickens; D008954:Models, Biological; D038081:Organogenesis / Q000502:physiology*; D014817:Vitelline Membrane / Q000502:physiology
axial rotation; biomechanics; embryonic development; left–right asymmetry; torsion