Sense of absence: Spatial perception through active sensing by insect antennal mechanosensory system

ABSTRACT Animals perceive their surroundings by using various modalities of sensory inputs to navigate their locomotion. Nocturnal insects such as crickets use mechanosensory inputs mediated by their antennae to navigate under dark conditions. Active sensing with voluntary antennal movements improves spatial information, but it remains unclear how accurately the insects can perceive the surrounding space by using their antennal system. Crickets exhibit escape behavior in response to a short air-puff, which is detected by the abdominal mechanosensory organ called cerci and is perceived as a “predator approach” signal. We placed objects of different shapes at different locations with which the cricket actively made contact using its antenna. We then examined the effects on wind-elicited escape. The crickets changed their movement trajectory depending on the shape and location of the objects so that they could avoid collision with these obstacles even when the escape behavior was triggered by another modality of stimulus. For instance, when a wall was placed in front of the crickets so that it was detected by one side of their antenna, the escape trajectory in response to a stimulus from behind was significantly biased toward the side opposite the wall. However, if the antenna on the free side without the wall was ablated, this modulation to avoid collision diminished, suggesting that the antenna on the free side provided information of “absence” of obstacles. This study demonstrated that crickets were able to perceive spatial information, including the presence or absence of objects by active sensing with their antennal system. Summary Statement Crickets can acquire spatial information such as shape, location and orientation of objects through active sensing by antennal mechanosensory system, which also provides information about the absence of objects.