Optimal decision making for sperm chemotaxis in the presence of noise

Abstract: For navigation, microscopic agents such as biological cells rely on noisy sensory input. In cells performing chemotaxis, such noise arises from the stochastic binding of signaling molecules at low concentrations. Using chemotaxis of sperm cells as application example, we address the classic problem of chemotaxis towards a single target. We reveal a fundamental relationship between the speed of chemotactic steering and the strength of directional fluctuations that result from the amplification of noise in the chemical input signal. This relation implies a trade-off between slow, but reliable, and fast, but less reliable, steering. By formulating the problem of optimal navigation in the presence of noise as a Markov decision process, we show that dynamic switching between reliable and fast steering substantially increases the probability to find a target, such as the egg. Intriguingly, this decision making would provide no benefit in the absence of noise. Instead, decision making is most beneficial, if chemical signals are above detection threshold, yet signal-to-noise ratios of gradient measurements are low. This situation generically arises at intermediate distances from a target, where signaling molecules emitted by the target are diluted, thus defining a `noise zone' that cells have to cross. Our work addresses the intermediate case between well-studied perfect chemotaxis at high signal-to-noise ratios close to a target, and random search strategies in the absence of navigation cues, e.g. far away from a target. Our specific results provide a rational for the surprising observation of decision making in recent experiments on sea urchin sperm chemotaxis. The general theory demonstrates how decision making enables chemotactic agents to cope with high levels of noise in gradient measurements by dynamically adjusting the persistence length of a biased persistent random walk.