Collective surfing of single cells on a chemo-attractant wave using multiscale Eulerian velocity vector field

Wavelike motion mediated by chemotactic signaling occurs in various biological phenomena including neutrophil swarms, wound healing, and amoeba aggregates. However, the macroscopic transition from independent to collective cellular behavior remains unclear, including how to quantify the response of individual cells to a developing chemotactic wave. Recent advances in molecular imaging allow concurrent observation of cyclic adenosine monophosphate (cAMP) concentrations and cell movement at individual resolution. Employing particle image velocimetry (PIV), a scheme to extract Eulerian velocity vector fields in fluids, we derived velocity fields at different Gaussian blurring levels and found that while original fluorescent images reflect cell movement, blurred versions highlight cAMP wave propagation. We identified the phase of cAMP signal wave dynamics and analyzed the interplay between single-cell motility and cAMP wave development. The extracted velocity fields at single-cell resolution show an almost antipodal relationship to those of the cAMP wave characterized by the blurred image, with an angle close to 180° during the rise of the wave when the spiral wave is well developed. Furthermore, single-cell dynamics collectively move toward the crest of the coming cAMP wave but rest (with randomized directionality) in the troughs between waves, akin to "surfing of the collectives".