• 2024 (Vol.38)
  • 1990 (Vol.4)
  • 1989 (Vol.3)
  • 1988 (Vol.2)
  • 1987 (Vol.1)

Frequency organization of the auditory receptor complex in midges (Chironomidae, Diptera)

© 2016 D. N. Lapshin

Institute for Information Transmission Problems of the RAS (Kharkevich Institute) 127051, Moscow, Bolshoy Karetny per, 19

Received 21 Apr 2015

"The main function of the auditory system in males of chironomid midges is believed to be the detec- tion of a conspecific female by the sound of its flight. In this study the frequency characteristics of the Johnston organ (JO) auditory receptors were measured electrophysiologically in midges (Chironomus plumosus). Responses of receptors were recorded from their axons in antennal nerve using glass microelectrode. Responses were amplified and fed to the stimulating loudspeaker, thus establishing the positive feedback stimulation. Characteristic frequencies of 436 individual receptor units were measured in this way. Further analysis revealed that, based on individual characteristic frequencies, the whole receptor complex of the JO can be divided into four distinct groups: A (160–190 Hz), B (205–245 Hz), C (255– 285 Hz) and D (315–370 Hz). The group С corresponds to the fundamental frequency produced by a conspecific female. Groups B and C fit into the best frequency range of the JO measured by other elec- trophysiological techniques. Frequency range of the group A coincides with the combination harmonic of the two frequencies: fundamental of a female flight tone and a male own flight tone. Most of the JO receptors formed pairs which were physiologically distinct in the antennal nerve. Sev- eral forms of multi-receptor responses were observed during autoexcitation: two different receptors, each one having its own characteristic frequency, responded in antiphase (with 0° and 180o phases of stimula- tion), and two receptors demonstrated simultaneous autoexcitation at same phase of stimulation. The first form was observed in ca. 60% of the whole number of recordings. In more than half of these cases the ratio between two frequencies was within a narrow range: 1.18–1.28 (average 1.24). Pairs of receptors with this frequency ratio belonged respectively to the groups A–B, B–C or C–D. In case of simultaneous multireceptor autoexcitation 25% of the pairs demonstrated the frequency ratio of ca. 1.5 and belonged to the groups A and C. This non-random and specific combination of frequencies in receptor pairs indicates that the auditory system of a midge utilizes the logic multiplication (conjunction) of different features of the conspecific signal. Functional coupling of differently tuned receptors, in part based on the principle of opponency (anti- phase pairs of receptors), might simplify and accelerate further signal processing in the brain."

Key words: Johnston organ, Chironomus plumosus, midge, acoustic communication, frequency tuning, positive feedback

Cite: Lapshin D. N. Chastotnaya organizatsiya retseptornogo kompleksa dzhonstonovogo organa komarov-zvontsov (chironomidae, diptera) [Frequency organization of the auditory receptor complex in midges (chironomidae, diptera)]. Sensornye sistemy [Sensory systems]. 2016. V. 30(1). P. 69-78 (in Russian).

References:

  • Zhantiev R.D., Fedorova M.V. Ultrastructure of Johnston’s organ in Chironomus plumosus L. (Diptera, Chironomidae) // Entomol. Review. 1999. V. 78 No 2. P. 287–295 [in Russian].
  • Zhantiev R.D., Fedorova M.V., Chukanov V.S., Esipovich N.G. Morphological and functional organization of Johnston’s organs and antennae of midges (Diptera, Chironomidae) // Sensornye Sistemy. 2001. V. 15. No 1. P. 73–84 [in Russian].
  • Zhantiev R.D., Fedorova M.V. Effect of air temperature on physiological characteristics of Jonston’s organ of midges (Diptera, Chironomidae) // Moscow University Biological Sciences Bulletin. 2003. Series 16. No 1. P. 32–37 [in Russian].
  • Lakin G.F. Biometry. Vysshaya shkola, 1990. Moscow, Russia. 352 p. [in Russian].
  • Lapshin D.N. Auditory perception in male mosquitoes (Diptera, Chironomidae) during flight simulation // Sensornye systemy. 2010. V. 24. No 2. P. 141–150 [in Russian].
  • Lapshin D.N. Frequency threshold curves of auditory interneurons of male mosquitoes Culex pipiens pipiens L. (Diptera, Culicidae) // Doklady Biological Sciences. 2011. V. 439. No 2. P. 279–282 [in Russian].
  • Lapshin D.N. Mosquito bioacoustics: auditory processing in males of Culex pipiens pipiens L. (Diptera, Culicidae) during flight simulation // Entomological Review. 2012. V. 91. No 1. P. 36–57 [in Russian].
  • Lapshin D.N. Frequency tuning of the auditory receptors in mosquitoes (Diptera, Chironomidae) // Sensornye systemy. 2013. V. 27. No 1. P. 35–46 [in Russian].
  • Tamarina N.A., Zhantiev R.D., Fedorova M.V. Flight tones and frequency characteristics of Johnston organ in sympatric species of Aedes mosquitoes // Parazitologiya. 1980. V. 14. P. 398–401 [in Russian].
  • Arthur B.J., Wyttenbach R.A., Harrington L.C., Hoy R.R. Neural responses to oneand two-tone stimuli in the hearing organ of the dengue vector mosquito. J. Experimental Biology. 2010. V. 213. P. 1376–1385.
  • Belton P. The physiology of sound reception in insects // Proc. Entomol. Soc. Ontario. 1962. V. 92. P. 20–26.
  • Belton P. An analysis of direction finding in male mosquitoes // Experimental Analysis of Insect Behaviour. Heidelberg, New York: Springer. 1974. P. 139–148.
  • Boo K.S., Richards A.G. Fine structure of the scolopidia in the Johnston’s organ of male Aedes aegypti (L.) (Diptera: Culicidae) // Internat. J. of Insect Morphol. Embryol.. 1975. V. 4. P. 549–566.
  • Charlwood J.D., Jones M.D.R. Mating in the mosquito Anopheles gambiae s.l. II. Swarming behaviour // Physiol. Entomol. 1980. V. 5. P. 315–320.
  • Daw N.W. Neurophysiology of color vision // Physiological Reviews Pub. 1973. V. 53. No 3. P. 571–611.
  • Gibson G., Warren В., Russell I. Humming in tune: sex and species recognition by mosquitoes on the wing // JARO. 2010. V. 11. P. 527–540.
  • Göpfert M.C., Briegel H., Robert D. Mosquito hearing: sound-induced antennal vibrations in male and female Aedes aegypti // J. Experimental Biology. 1999. V. 202. P. 2727–2738.
  • Ignell R., Dekker T., Ghaninia M., Hansson B S. Neuronal architecture of the mosquito deutocerebrum // J. Comparative Neurology. 2005. V. 493. P. 207–240.
  • Jackson J.C., Robert D. Nonlinear auditory mechanism enhances female sounds for male mosquitoes // Proc. Natl. Acad. Sci. USA. 2006. V. 103. No 45. P. 16734– 16739.
  • Johnston C. Auditory apparatus of the Culex mosquito // Q. J. Microsc. Sci. 1855. V. 3. P. 97–102.
  • Lapshin D.N., Vorontsov D.D. Frequency tuning of individual auditory receptors in female mosquitoes (Diptera, Culicidae) // J. Insect Physiology. 2013. V. 59. P. 828–839.
  • Ogawa K., Sato H. Relationship between male acoustic response and female wingbeat frequency in a chironomid midge, Chironomus yoshimatsui (Diptera : Chironomidae) // Jpn. J. Sanit. Zool. 1993. V. 44. No 4. P. 355– 360.
  • Römer F. Einfluss von Temperatur und Alter auf die Flugtonhöhe beim Schwärmen von Chironomus plumosus L. // Revue Suisse de Zoologie. 1970. B. 77. S. 603– 616.
  • Roth L.M. A study of mosquito behavior. An experimental laboratory study of the sexual behaviour of Aedes aegypti Linnaeus // Amer. Midi. Naturalist. 1948. V. 40. P. 265–352.
  • Tischner H. Über den Gehörsinn von Steckmücken // Acustica Suisse. 1953. Bd. 3. S. 335–343.
  • Tischner H., Schief A. Fluggeräusch und Schallwahrnehmung bei Aedes aegypti L. (Culicidae) // Zoologischer Anzeiger. 1955. Bd. 18 (Suppl. ). S. 453–460.
  • Warren В., Gibson G., Russell I.J. Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion // Current Biol. 2009. V. 19. P. 485–491.
  • Wishart G., Riordan D.F. Flight responses to various sounds by adult males of Aedes aegypti // Canadian Entomologist. 1959. V. 91. P. 181–191.