Frequency organization of the Johnston organ in male mosquitoes (Diptera, Culicidae)

Abstract

The Johnston's organs (JO) of mosquitoes are the most complex mechanosensitive organs yet found in insects. Previous findings on the behavior of mosquitoes suggest that, together with exceptional sensitivity, their auditory system can discriminate frequencies. Analysis of compound responses of the JO did not provide unambiguous evidence of such discrimination, nor did it help to find its mechanism. Using the feedback stimulation method, we measured the tuning frequencies of the JO sensory neurons. Here we present electrophysiological evidence that male mosquitoes of possess at least eight groups of auditory neurons that are distinct in their frequency tuning, with individual frequencies ranging from 85 to 470 Hz. Most of the neurons are tuned to 190-270 Hz, which corresponds to the difference between male and female flight tones. Axons of the JO sensory units propagate graded amplified receptor potentials rather than all-or-none action potentials, are grouped into pairs or triplets and often respond in anti-phase to each other. Some features of the mosquito auditory system suggest an analogy to the retinal mechanisms. Together with our previous findings on frequency tuning in female mosquitoes of different species, this study presents evidence in favor of sophisticated frequency analysis of sound in mosquitoes.

Directional and frequency characteristics of auditory neurons in Culex male mosquitoes

“…Remarkably, almost similar frequency ratios between the paired flight tones of male and female mosquitoes were observed (Aldersley et al, 2016). Such tendency may also explain the multi-modal shape of overall distribution of individual frequencies, which was demonstrated in our previous study (Lapshin and Vorontsov, 2017).…”

“…The examples of individual responses are shown in Fig.2. We do not show the waveforms here, they were similar to the ones descibed in detail elsewhere (Lapshin and Vorontsov, 2017).…”

“…The first finding which that study brought was the difference in frequency tuning between the JO sensory neurons both in female (Lapshin and Vorontsov, 2013) and male mosquitoes (Lapshin and Vorontsov, 2017). It was rather expected, keeping in mind the high number of units and also the behavioral observations which implied the frequency discrimination in mosquitoes (Aldersley and Cator, 2019;Aldersley et al, 2016;Lapshin and Vorontsov, 2018;Simões et al, 2016;Simões et al, 2018).…”

“…Such cumulative effect led to the formation of a series of mixed harmonics in the recording. When the ratio between the frequencies was close to 1.5 (3/2, one of the peaks in the distribution in Fig.5B), the resulting spectrum became similar to a single harmonic series, like in zone at the same frequency, appearing after the rotation of the stimulation vector by 180°, thus converting the positive feedback to the negative one for a given unit (Lapshin and Vorontsov, 2017). Figure 5B shows the distribution of frequency ratio F 3 /F 2 from the triple systems (n=30).…”

“…For the sake of simplicity, here we use the terms 'unit' or 'sensory unit' in the sense of one or several axons belonging to the primary sensory neurons of the JO, closely located within the antennal nerve and sharing similar frequency and phasic properties, thus representing a single functional unit. Detailed discussion of this issue can be found elsewhere (Lapshin and Vorontsov, 2013;Lapshin and Vorontsov, 2017)…”