Auditory System of Blood-Sucking Mosquitoes (Diptera, Culicidae)

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Abstract

This review comprehensively explores the morphology of the mosquito auditory organs – antennae and Johnston’s organs. Spatial and frequency characteristics of auditory sensory neurons within Johnston’s organs are discussed, as well as the mechanisms of mechanotransduction in these neurons. The review presents findings from studies investigating the aspects of mosquito perception of acoustic signals when their auditory system is subjected to vibrations generated by flapping wings. Additionally, the review discusses the significance of acoustic communication in the reproductive behavior of mosquitoes.

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About the authors

D. N. Lapshin

Institute for Information Transmission Problems (Kharkevich Institute)

Author for correspondence.
Email: lapshin@iitp.ru
Russian Federation, Moscow

References

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2. Fig. 1. Photographs of antennae and johnston organs: a - male, b - female. Denotations: ant - antenna, do - johnston's organ

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3. Fig. 2. Schematic diagram of the jejunal organ (according to Hart et al., 2011 with modifications)

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4. Fig. 3. Activity in the antennal nerve axon: the moment of transition from extracellular to intracellular registration (a, upper oscillogram) against the background of the action of tonal stimulating messages (a, lower oscillogram). The moment of transition corresponds to a negative potential jump. Response to acoustic stimulation registered in the axon of an auditory receptor at intracellular withdrawal (b, upper oscillogram). Stimulus frequency 320 Hz, amplitude 50 dB SPVL (b, lower oscillogram)

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5. Fig. 4. Schematic of the structure of sensilla of type A of the Johnston organ of the male mosquito (figure according to Boo, Richards, 1975a, with modifications)

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6. Fig. 5. Positive feedback: a - generalised block diagram of the system covered by the positive feedback loop, the formula of the transfer coefficient of such a system is given in the figure to the right of the block diagram. The main channel of the system with initial transfer coefficient K0 > 1, the signal from its output through the positive feedback block with transfer coefficient B < 1 is summed (+) with the input signal of the system. When the product K0∙B → 1 Cos → ∞ is approached. b - simplified scheme of the mechanotransduction module consisting of one ion channel, an adaptation molecular motor and an elastic element (figure according to Nadrowski et al., 2008 with modifications); positive feedback is provided by the release of calcium ions when the receptor membrane is stretched; c - changes in the shape of the tuning curve of the frequency-selective element under the action of positive feedback: increase in the gain at the optimal frequency, sharpening of the tuning curve of the frequency-selective element at the optimum frequency, sharpening of the tuning curve at the optimum frequency.

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7. Fig. 6. Spectra of electrical activity in the antennal nerve against the background of feedback action in the acoustic stimulation channel: a - autoexcitation at 154 Hz in the positive feedback mode; b - local suppression of noise when the phase of the feedback signal is inverted (i.e., when negative feedback is applied) at the frequency where autoexcitation was previously observed. Female Aedes excrucians, figure from (Lapshin, Vorontsov, 2013) with modifications

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8. Fig. 7. Directional diagrams of auditory receptors of the left DO of Culex pipiens pipiens females measured during stimulation in a feedback loop: a - directional diagram of a single receptor consisting of one unipolar lobe (autoexcitation frequency 112 Hz); b - diagrams of two receptors (tuning frequencies 104 Hz and 77 Hz), the activity of which was simultaneously registered in the same area of the antennal nerve. Receptors in this pair reacted in antiphase to acoustic stimulation; in the autoexcitation mode their diagrams are directed in opposite directions. The inset with the mosquito image (back view) shows the zero position and the direction of the positive reference of the angular coordinate j. The relative sensitivity (the inverse of the autoexcitation threshold) is plotted along the radius of the diagrams. Figure from (Lapshin, Vorontsov, 2023) with modifications

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9. Fig. 8. Histogram of distribution of frequencies of autoexcitation (characteristic frequencies) of auditory receptors of DOs of male Culex pipiens pipiens mosquitoes. Vertical axis - number of registered receptors with characteristic frequencies within one 5 Hz bin. The horizontal bracket with the sign ♀ indicates the range of variability of the basic flight tones of conspecific females. Peaks combining data for receptors that responded in antiphase to the bulk of cells tested are shaded in grey. Figure according to (Lapshin, Vorontsov, 2017) with modifications

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10. Fig. 9. Family of audiograms of narrowband auditory receptors. Data from electrophysiological experiments with male Aedes communis. Numbers at each curve indicate the corresponding value of goodness of fit at +6 dB from the threshold minimum (Q6). Figure according to (Lapshin, Vorontsov, 2019) with modifications

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11. Fig. 10. Frequency rearrangement of the auditory system of male Culex pipiens pipiens mosquitoes after injection of octopamine into insect haemolymph. Figure according to (Vorontsov, Lapshin, 2023; Vorontsov, Lapshin, 2024) with modifications

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12. Fig. 11. Frequency spectrum of electrical activity recorded in the antennal nerve of male Aedes communis in response to sinusoidal stimulation (200 Hz) against the background of flight simulation (frequency 433 Hz). The spectrum contains peaks of the first (200 Hz) and second harmonics (400 Hz), constituting the receptor response directly to the sinusoidal stimulus, 433 Hz and 866 Hz - the first and second harmonics corresponding to the frequency of flight simulation. In addition to these peaks, the spectrum contains Raman harmonics 433 - 200 = 233 (Hz) and 433 + 200 = 633 (Hz), with the 233 Hz difference harmonic being 7 dB greater in amplitude compared to the response to the sinusoidal stimulus (200 Hz harmonic). If the preparation was stimulated with a 633 Hz sinusoidal signal (i.e., in the mirror channel region) against the background of a flight simulation, the 633 - 433 = 200 (Hz) difference combinational harmonic was formed in the region of maximum sensitivity of the auditory receptors. Figure according to (Lapshin, Vorontsov, 2021) with modifications

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13. Fig. 12. Audiograms constructed from the data of electrophysiological (a) and behavioural experiments (b). The position of the mirror channel (in the 600 Hz region) is indicated by arrows. Flight sound spectra of conspecific females (♀) and males (♂) are superimposed on the graphs. a: results of testing of Culex pipiens pipiens males in stationary conditions and against the background of flight simulation (Lapshin, 2012a; Lapshin, 2012); b: results of swarm stimulation of Aedes communis males in natural conditions (Lapshin, Vorontsov, 2021). In the 350-500 Hz range, no behavioural responses to stimuli with a level of 90 dB SPL or less were recorded

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14. Fig. 13. Histogram of distribution of frequencies of autoexcitation (characteristic frequencies) of auditory receptors of DOs of female Culex pipiens pipiens mosquitoes. Vertical axis - number of registered receptors with characteristic frequencies within one 5 Hz bin (Lapshin, Vorontsov, 2013)

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15. Fig. 14. Examples of audiograms of narrowband auditory receptors of female Culex pipiens pipiens. Numbers at each curve indicate the Q6 goodness-of-fit value. Figure according to (Lapshin, Vorontsov, 2023) with modifications

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16. Fig. 15. Increase of acoustic thresholds in the frequency range below 90 Hz after octopamine injection to female Culex pipiens pipiens mosquitoes (Vorontsov, Lapshin, 2023; Vorontsov, Lapshin, 2024)

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17. Fig. 16. Distribution of spatial orientation parameters (angle φ) and minimum thresholds (Th, dB) of receptors of the left DO of Culex pipiens pipiens females presented in polar coordinates (Lapshin, Vorontsov, 2023). Threshold values in the ratio ‘lower threshold - larger radius’ (a measure of auditory sensitivity) are plotted along the radius of the diagram. Each pair of diametrically located coloured circles corresponds to the results of testing one receptor (such data representation follows from the symmetrical-bipolar diagram of receptor orientation during the perception of sinusoidal signals). It should be noted that the sensory neurons of the left DO were mostly oriented in quadrants I and III (0-90 and 180-270°); the average value of the angular orientation of the most sensitive receptors in these quadrants is φ = 53° (indicated in the figure by a vector). The histogram of distribution of auditory receptor thresholds in DO females is shown in the inset below

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18. Fig. 17. Spatial model of the system of directional diagrams of two symmetric groups of receptors of the left (L1) and right (R1) DOs (top view) oriented at an angle φ = 53°. The similarly shaped symmetrical regions of the L2 and R2 diagrams are not shown to simplify the figure (Lapshin and Vorontsov, 2023). The active zone of comparison of signals from the receptors of the right and left DOs is shown in grey in the area of intersection of the diagrams. The width of this zone is determined by the angle 2ξ between the mosquito antennas (inset in the figure on the left): as the angle 2ξ increases, the mutual overlap of the zones in front of the insect also increases. The figure shows the results of the modelling of the overlap zones for two typical values of the angle between the antennas (55 and 73.9°)

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