In nature, animals need to perceive various signals. Olfactory signals are diverse, and insects recognize and utilize them to locate resources such as mates, food, and oviposition sites. However, olfactory signals are often complex, including signals that attract them and signals that trigger avoidance or escape.

When the population density of migratory locusts (Locusta migratoria) is high, they can form massive swarms while releasing the aggregation pheromone 4VA and the aposematic signal PAN. 4VA attracts locust individuals to gather and form swarms, whereas PAN deters conspecifics to avoid cannibalism and repel predators. When locusts perceive both compounds simultaneously, how do they reconcile the behaviors of aggregation and repulsion?

Research Team led by Prof. KANG Le from the Institute of Zoology of the Chinese Academy of Sciences, has discovered that migratory locusts achieve a delicate balance between swarm aggregation, predator defense, and cannibalism avoidance through sophisticated neural modulation of two conflicting olfactory signals: the aggregation pheromone 4-vinylanisole (4VA) and the alarm pheromone phenylacetonitrile (PAN). These significant findings were published in the PNAS.

This study addresses this by examining the release dynamics of the two signals, their behavioral effects, and the neural mechanisms underlying their perception.

Under the same duration of crowding treatment, 4VA is released at significantly lower locust densities (4-5 locusts) compared to PAN (which requires 16-17 solitary locusts). At equivalent population densities, 4VA release initiates earlier (after 24 h) than PAN release (after 48 h), while PAN progressively becomes the main component during the aggregation process.

Although PAN’s emission levels eventually exceed those of 4VA, locusts consistently exhibit a preference for the emitted blend, regardless of variations in proportions and concentrations. Notably, increasing amounts of 4VA added to PAN can counteract PAN’s repellent effects, but this is not the case when PAN is added to 4VA.

Why 4VA dominates the behavioral responses of locusts to the mixture? The researchers measured the electrophysiological responses in antennae, and discovered that antennal neurons responsive to 4VA suppress the activity of neurons responsive to PAN. 

In the antennal lobe, the researchers found that the spatio-temporal patterns of PNs in response to mixture show similarity to that of 4VA rather than those of PAN. Further investigation revealed that the conduction velocities of projection neurons, rather than other neural properties, drive the observed behavioral pattern, resulting in an overall attractive response.

The study not only provides novel insights into animal behavioral decision-making processes, but also reveals fundamental neural mechanisms for resolving conflicting sensory information in nature. The study demonstrates how neural circuits implement an optimal strategy that simultaneously promotes population expansion while minimizing survival risks.

Figure：The synergistic interactions between 4VA and PAN across multiple levels facilitate locust attraction and aggregation.（Image by Prof. KANG Le’ Lab）