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Journal of comparative physiology

, Volume 127, Issue 1, pp 11–28 | Cite as

Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L.,Gryllus bimaculatus DeGeer)

  • David W. Wohlers
  • Franz Huber
Article

Summary

Intracellular recording and staining techniques have been used to investigate physiological and anatomical properties of two kinds of auditory interneurons in the prothoracic ganglion of the crickets,Gryllus campestris L. andGryllus bimaculatus DeGeer: a segmental interneuron (the omega cell) and an auditory interneuron with an ascending axon (AIAA).

Using cobalt-nitrate-filled electrodes we were able to study physiological features for periods as long as 10 min following penetration and simultaneously stain the cell. With potassium-acetate electrodes, similar intracellular recordings lasted longer than an hour.
  1. 1.

    The omega cell is a large segmental auditory neuron with four branching areas (fields A, B, C, D). Two such cells are found in the prothoracic ganglion, as mirror images of one another.

     
  2. 2.

    The omega cell receives its auditory input entirely from the cell-body side. EPSPs as well as spike activity are seen in the large dendritic root of field A; the spikes are conducted to the contralateral side of the neuron and invade fields C and D, which are considered to be output areas of the neuron.

     
  3. 3.

    When the two ears are isolated acoustically, allowing separate stimulation of the tympana, it appears that the two omega cells inhibit one another mutually. They may, therefore, participate in the neuronal mechanism involved in directional sensitivity.

     
  4. 4.

    The omega cell is best tuned to the carrier frequency of the conspecific song, but exhibits a secondary threshold minimum in the region of the higher harmonics. The response is linearly related to the log of the sound intensity, as found in the auditory afferents.

     
  5. 5.

    The temporal pattern of the cricket calling song is well copied by the omega cell. No optimal “tuning” to specific syllable durations, syllable periods or verse durations was observed. Maintained tones elicit a tonic response and sound envelopes are mimicked by both subthreshold and spike-activity.

     
  6. 6.

    The auditory interneuron with ascending axon (AIAA) has a dendritic field and ascending axon restricted almost entirely to one hemisphere of the prothoracic ganglion; the cell body is located in the anterior contralateral hemisphere.

     
  7. 7.

    The AIAA exhibits IPSPs highly synchronized in response to sounds presented at the carrier frequency. At sound frequencies above 10 kHz the AIAA is activated, but the responses to the syllables of the calling song are not as sharply separated as in the omega cell.

     
  8. 8.

    Latencies of AIAA spike activity are comparable to those in the omega cell and suggest that both cells are first order interneurons.

     
  9. 9.

    The frequency-dependence of excitation and inhibition in the AIAA make it a candidate element of a neuronal process that might modify response to the calling song in the presence of the courtship song.

     

Keywords

Intracellular Recording Auditory Neuron Courtship Song Calling Song Tonic Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviation

AIAA

auditory interneuron (with an) ascending axon

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References

  1. Bacon, J.P., Altman, J.S.: A silver intensification method for cobalt-filled neurons in wholemount preparations. Brain Res.138, 359–363 (1977)Google Scholar
  2. Bentley, D.: Intracellular activity in cricket neurons during generation of song patterns. Z. vergl. Physiol.62, 267–283 (1969)Google Scholar
  3. Burrows, M.: The role of delayed excitation in the coordination of some metathoracic flight motoneurons of a locust. J. comp. Physiol.83, 135–164 (1973)Google Scholar
  4. Burrows, M.: Monosynaptic connexions between wing stretch receptors and flight motoneurones of the locust. J. exp. Biol.62, 189–219 (1975)Google Scholar
  5. Casaday, G.B., Hoy, R.R.: Auditory interneurons in the cricketTeleogryllus oceanicus: physiological and anatomical properties. J. comp. Physiol.121, 1–13 (1977)Google Scholar
  6. Eibl, E.: Morphologische und neuroanatomische Untersuchungen zur Sinnesorganausstattung der proximalen Tibienabschnitte und ihrer zentralen Projektionen bei Grillen. Dissertation, Universität zu Köln, Köln 1976Google Scholar
  7. Eibl, E., Huber, F.: Tympanal nerve fibers in the cricketsGryllus campestris L. andGryllus bimaculatus DeGeer: Projections in the prothoracic ganglia, as compared with those of homologous meso- and metathoracic nerves. Zoomorphologie, in press (1978)Google Scholar
  8. Elepfandt, A.: Auditory interneurons in the mesothoracic ganglion of the cricket,Gryllus bimaculatus DeGeer. Verb. Deutsch. Zool. Ges. 71. Jahrestagung, Konstanz, 1978Google Scholar
  9. Elsner, N., Popov, A.V.: Neuroethology of acoustic communication. Adv. Insect Physiol.13, 229–335 (1978)Google Scholar
  10. Erber, J., Menzel, R.: Visual interneurons in the median protocerebrum of the bee. J. comp. Physiol.121, 65–77 (1977)Google Scholar
  11. Esch, H., Huber, F., Wohlers, D.: Physiological and anatomical characteristics of single sensory auditory units in crickets (Gryllus campestris L. andGryllus bimaculatus DeGeer), in preparation (1978)Google Scholar
  12. Fielden, A.: Transmission through the last abdominal ganglion of the dragonfly nymph,Anax imperator. J. exp. Biol.37, 832–844 (1960)Google Scholar
  13. Hagiwara, S., Watanabe, A.: Discharges in motoneurons of cicada. J. Cell. Comp. Physiol.47, 415–428 (1956)Google Scholar
  14. Hausen, K.: Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowflyCalliphora erythrocephala. Z. Naturforsch.31 c, 629–633 (1976)Google Scholar
  15. Hill, K.: Acoustic communication in the Australian field cricketsTeleogryllus commodus andT. oceanicus (Orthoptera: Gryllidae). Ph. D. thesis. University of Melbourne, Melbourne, Australia 1974Google Scholar
  16. Hill, K.G., Boyan, G.S.: Directional hearing in crickets. Nature262, 390–391 (1976)Google Scholar
  17. Hill, K.G., Boyan, G.S.: Sensitivity to frequency and direction of sound in the auditory system of crickets (Gryllidae). J. comp. Physiol.121, 79–97 (1977)Google Scholar
  18. Huber, F.: Lautäußerungen und Lauterkennen bei Insekten (Grillen). 26. Jahresfeier Rheinisch Westfälische Akademie der Wissenschaften: N265, 15–66. Opladen: Westdeutscher Verlag 1977Google Scholar
  19. Huber, F., Stout, J.F.: Coding of sound patterns by ascending neurons in the auditory pathway of the cricket,Gryllus campestris L. Verh. Deutsch. Zool. Ges. 71. Jahrestagung, Konstanz, 1978Google Scholar
  20. Kalmring, K.: The afferent auditory pathway in the ventral cord ofLocusta migratoria (Acrididae). I. J. comp. Physiol.104, 103–141 (1975)Google Scholar
  21. Kater, S.B., Nicholson, C.: Intracellular staining in neurobiology, Berlin-Heidelberg-New York: Springer 1973Google Scholar
  22. Kien, J.: A preliminary report on cobalt sulphide staining of locust visual interneurones through extracellular electrodes. Brain Res.109, 158–164 (1976)Google Scholar
  23. Larsen, O.N., Michelsen, A.: Biophysics of the ensiferan ear III. The cricket ear as a four-input system. J. comp. Physiol.123, 217–227 (1978)Google Scholar
  24. Nocke, H.: Physiological aspects of sound communication in crickets (Gryllus campestris L.). J. comp. Physiol.80, 141–162 (1972)Google Scholar
  25. Paton, J.A., Capranica, R.R., Dragsten, P.R., Webb, W.W.: Physical basis for auditory frequency analysis in field crickets (Gryllidae). J. comp. Physiol.119, 221–240 (1977)Google Scholar
  26. Pearson, K.G., Fourtner, C.R.: Nonspiking interneurons in walking system of the cockroach. J. Neurophysiol.38, 33–52 (1975)Google Scholar
  27. Popov, A.V.: Frequency selectivity of the reaction of auditory neurons in the 1st thoracic ganglion of the cricketGryllus bimaculatus DeGeer. Jurnal Evol'uzionnoj Biochimii i Fiziologii9, 265–277 (1973)Google Scholar
  28. Popov, A.V., Shuvalov, V.F., Svetlogorskaya, I.D., Markovich, A.M.: Acoustic behavior and auditory system in insects. In: Mechanoreception (ed. J. Schwartzkopff): Rheinisch Westfälische Akad. d. Wiss., Abh.,53, 281–306 (1974)Google Scholar
  29. Rehbein, H.G.: Auditory neurons in the ventral cord of the locust: morphological and functional properties. J. comp. Physiol.110, 233–250 (1976)Google Scholar
  30. Rehbein, H.G., Kalmring, K., Römer, H.: Structure and function of acoustic neurons in the thoracic ventral nerve cord ofLocusta migratoria (Acrididae). J. comp. Physiol.95, 263–280 (1974)Google Scholar
  31. Rheinlaender, J., Kalmring, K., Popov, A.V., Rehbein, H.G.: Brain projections and information processing of biologically significant sounds by two large ventral cord neurons ofGryllus bimaculatus DeGeer (Orthoptera, Gryllidae). J. comp. Physiol.110, 251–269 (1976)Google Scholar
  32. Stout, J.F., Huber, F.: Responses of central auditory neurons of female crickets (Gryllus campestris L.) to the calling song of the male. Z. vergl. Physiol.76, 302–313 (1972)Google Scholar
  33. Stout, J.F., Huber, F.: Pattern coding in some ascending auditory neurons ofGryllus campestris L, in preparation (1978)Google Scholar
  34. Suga, N.: Central mechanism of hearing and sound localization in insects. J. Insect Physiol.9, 867–873 (1963)Google Scholar
  35. Tyrer, N.M., Bell, E.M.: The intensification of cobalt-filled neuron profiles using a modification of Timm's sulphide-silver method. Brain Res.73, 151–155 (1974)Google Scholar
  36. Weber, T.: Comparative aspects of the calling songs in three cricket species with respect to species specific recognition in female phono taxis. Verh. Deutsch. Zool. Ges. 71 Jahrestagung, Konstanz, 1978Google Scholar
  37. Wiese, K.: Temporal and spatial filtering by the omega neuron in the acoustic ascending pathway ofGryllus bimaculatus DeGeer, in preparation (1978)Google Scholar
  38. Wohlers, D., Huber, F.: Anatomical and physiological characterization of intracellularly recorded and stained acoustical neurons inGryllus campestris L. andGryllus bimaculatus DeGeer. Verh. Deutsch. Zool. Ges. 71 Jahrestagung, Konstanz, 1978Google Scholar
  39. Zaretsky, M.D.: Patterned response to song in cricket central auditory neurone. Nature229, 195–196 (1971)Google Scholar
  40. Zhantiev, R.D., Kalinkina, I.N., Tshukanov, V.S.: The characteristics of the directional sensitivity of tympanal organs inGryllus bimaculatus DeGeer (Orthoptera, Gryllidae). Entomol. Obozr.54, 249–256 (1975a)Google Scholar
  41. Zhantiev, R.D., Kalinkina, I.N., Tshukanov, V.S.: Functional characteristics of two auditory interneurons in the cricketGryllus bimaculatus DeGeer (Orthoptera, Gryllidae). Vestnik MGU, Ser. Biol.6, 18–25 (1975b)Google Scholar
  42. Zhantiev, R.D., Kalinkina, I.N.: Sound reaction of descending neurons in the abdominal central nervous system. Nauchn(ye) dokl(ady) vysshei shkoly20, biol. nauki, No. 8, 66–71 (1977)Google Scholar
  43. Zhantiev, R.D., Korsunovskaya, O.S.: Reaction to sound of descending neurons in cervical connectives of the cricketGryllus bimaculatus DeGeer (Orthoptera, Gryllidae). Entomol. obozr.54, 248–257 (1977)Google Scholar
  44. Zhantiev, R.D., Tshukanov, V.S.: Frequency characteristics of tympanal organs of the cricketGryllus bimaculatus DeGeer (Orthoptera, Gryllidae). Vestnik MGU, Ser. Biol.2, 3–8 (1972a)Google Scholar
  45. Zhantiev, R.D., Tshukanov, V.S.: Reaction of the auditory system ofGryllus bimaculatus (Orthoptera, Gryllidae) to intraspecific sound signals. Zool. J.51, 983–993 (1972b)Google Scholar

Copyright information

© Springer-Verlag 1978

Authors and Affiliations

  • David W. Wohlers
    • 1
  • Franz Huber
    • 1
  1. 1.Abteilung HuberMax Planck Institut für VerhaltensphysiologieSeewiesenFederal Republic of Germany

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