Mapping the Auditory Space of Culex pipiens Female Mosquitoes in 3D

SIMPLE SUMMARY: Mosquitoes possess one of the best-developed and sensitive hearing systems among insects. Their auditory Johnston’s organs located at the antennae bases include several thousand radially distributed sensory cells. Male mosquitoes use their hearing for acoustic courtship behavior, while the function of hearing in blood-sucking female mosquitoes is poorly studied. In addition to courtship behavior, hearing is presumed to be used for host detection, including the use of human voices as an attraction cue. Since mosquitoes spread dangerous diseases such as West Nile fever, understanding their hearing system is of crucial importance. We studied the auditory system of Culex pipiens female mosquitoes using behavioral and electrophysiological experiments and created a three-dimensional model of the mosquito auditory space. The in-flight position of antennae was found optimal for binaural hearing focused primarily in front of, above and below a mosquito. By varying the antennae position a mosquito can adjust the directional properties of hearing depending on behavioral context. According to our findings, the auditory system of female mosquitoes has enough resolution to estimate the direction to the sound source, while its frequency range enables detection of sounds produced by other flying mosquitoes and human hosts. ABSTRACT: The task of directional hearing faces most animals that possess ears. They approach this task in different ways, but a common trait is the use of binaural cues to find the direction to the source of sound. In insects, the task is further complicated by their small size and, hence, minute temporal and level differences between two ears. A single symmetric flagellar particle velocity receiver, such as the antenna of a mosquito, should not be able to discriminate between the two opposite directions along the vector of the sound wave. Paired antennae of mosquitoes presume the usage of binaural hearing, but its mechanisms are expected to be significantly different from the ones typical for the pressure receivers. However, the directionality of flagellar auditory organs has received little attention. Here, we measured the in-flight orientation of antennae in female Culex pipiens pipiens mosquitoes and obtained a detailed physiological mapping of the Johnston’s organ directionality at the level of individual sensory units. By combining these data, we created a three-dimensional model of the mosquito’s auditory space. The orientation of the antennae was found to be coordinated with the neuronal asymmetry of the Johnston’s organs to maintain a uniformly shaped auditory space, symmetric relative to a flying mosquito. The overlap of the directional characteristics of the left and right sensory units was found to be optimal for binaural hearing focused primarily in front of, above and below a flying mosquito.