The human sperm head spins with a conserved direction during swimming in 3D

Abstract

In human sperm, head spinning is essential for sperm swimming and critical for fertilization. Measurement of head spinning has not been straightforward due to its symmetric head morphology, its translucent nature and fast 3D motion driven by its helical flagellum movement. Microscope image acquisition has been mostly restricted to 2D single focal plane images limited to head position tracing, in absence of head orientation and rotation in 3D. To date, human sperm spinning has been reported to be mono or bidirectional, and even intermittently changing direction. This variety in head spinning direction, however, appears to contradict observations of conserved helical beating of the human sperm flagellum. Here, we reconcile these observations by directly measuring the head spinning movement of freely swimming human sperm with multi-plane 4D microscopy. We show that 2D microscopy is unable to distinguish the spinning direction in human sperm. We evaluated the head spinning of 409 spermatozoa in four different conditions: in non-capacitating and capacitating solutions, for both aqueous and viscous media. All spinning spermatozoa, regardless of the experimental conditions spun counterclockwise (CCW) as seen from head-to-tail. Head spinning was suppressed in 57% of spermatozoa swimming in non-capacitating viscous media, though, interestingly, they recovered the CCW spinning after incubation in capacitating conditions within the same viscous medium. Our observations show that the spinning direction in human sperm is conserved, even when recovered from non-spin, indicating the presence of a robust and persistent helical driving mechanism powering the human sperm flagellum, thus of critical importance in future sperm motility assessments, human reproduction research and microorganism self-organised swimming.

Time and power dependence of laser-induced photodamage on human sperm revealed by longitudinal rolling measurement using optical tweezers

“…1(a) , Fig. 3(c) and ), which is consistent with our previous report [ 19 ], as well as a recent study on freely swimming sperm by Gabriel Corkidi et al [ 27 ]. Such unidirectional rolling may be associated with the special mechanical transmission structure in the sperm neck, i.e., the dynamic basal complex of the sperm flagellum [ 20 ], as the basal complex bends in response to the beating force of flagellum [ 28 ].…”

Swimming by spinning: spinning-top type rotations regularize sperm swimming into persistently symmetric paths in 3D

“…Indirect inference of the body orientation from observed flagellar path in 3D has been employed as an alternative [34,67], though more research is needed to determine whether this approach can confidently resolve the complex rotational movement of the sperm body frame in 3D. We hope that these results will motivate further advances on high-precision and direct measurements of microorganisms' body orientation in 3D [65,68].…”

“…Large errors may arise from tracking 2D projections of 3D sperm movements. This is particularly important as current CASA measurements are restricted to 2D visualizations of the sperm swimming trajectories due to the limitations of imaging techniques [15,31,68,71], and thus carry subsequent challenges on the potential misclassification of sperm motility [72].…”