Abstract
The ability of animals to effectively locate and navigate toward food sources is central for survival. Here, using C. elegans nematodes, we reveal the neural mechanism underlying efficient navigation in chemical gradients. This mechanism relies on the activity of two types of chemosensory neurons: one (AWA) coding gradients via stochastic pulsatile dynamics, and the second (AWCON) coding the gradients deterministically in a graded manner. The pulsatile dynamics of the AWA neuron adapts to the magnitude of the gradient derivative, allowing animals to take trajectories better oriented toward the target. The robust response of AWCON to negative derivatives promotes immediate turns, thus alleviating the costs incurred by erroneous turns dictated by the AWA neuron. This mechanism empowers an efficient navigation strategy that outperforms the classical biased-random walk strategy. This general mechanism thus may be applicable to other sensory modalities for efficient gradient-based navigation.
Highlights
Animals heavily rely on efficient detection of chemical cues to guide them in critical processes, such as detection of food or danger evasion
Shimomura et al.[8] demonstrated that C. elegans worms modulate the probability to perform a pirouette based on the sign of the first derivative of the sensed stimulus[8], to the classical biased-random walk strategy observed in single-cell organisms
To systematically study neural responses to continuously changing chemical gradients, we developed a microfluidics-based system that can present C. elegans nematodes with a wide range of smooth gradient shapes (Fig. 1a, see Supplementary Note 1 for details)
Summary
Animals heavily rely on efficient detection of chemical cues to guide them in critical processes, such as detection of food or danger evasion. Chemotaxis of C. elegans nematodes is comprised of long periods of sinusoidal movement, termed ‘runs’, and intermittent turning events, where a bout of consecutive turns is known as a ‘pirouette’[6,7,8] In their seminal work, Shimomura et al.[8] demonstrated that C. elegans worms modulate the probability to perform a pirouette based on the sign of the first derivative of the sensed stimulus[8], to the classical biased-random walk strategy observed in single-cell organisms. C. elegans worms are frequently recovered from rotting fruits[36], which constitute a secluded and turbulent-free environment, where abrupt changes in concentrations are presumably uncommon In such settings, stable gradients may be formed due to diffusion from bacterial microenvironments or food deteriorating signals[37]. Both AWA and AWC are connected to first-layer interneurons (e.g., AIY and AIA) that control worm navigation[39,43,44,45]
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