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Primary auditory neurons in crickets: Physiology and central projections

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Summary

  1. 1.

    The tibial tympanal organs ofGryllus campestris L. andGryllus bimaculatus DeGeer were stimulated with sound signals simulating the natural calling song, produced by sinusoidal amplitude envelope, using carrier frequencies (CF) in the range of 2–20 kHz at various intensities.

  2. 2.

    Glass microelectrodes (filled with 3 M potassium acetate, or with 1 M cobalt nitrate for marking the fibers) were used to record extracellularly or quasi intracellularly the spike activity of single sensory fibers in the leg nerve (Fig. 1) responding to acoustic stimuli and to stain their central projections within the prothoracic ganglion (Figs. 6–9).

  3. 3.

    The temporal pattern of the sound stimulus —syllable and verse structure — is reflected in the discharge pattern of the fibers studied (Figs. 1, 6, 7).

  4. 4.

    Five types of fibers tuned to specific CFs were found (Fig. 2). These had peak sensitivities (a) at 4–5 kHz (CF of the species calling song), (b) at both 4–5 and 10–12 kHz, (c) below 2 kHZ, (d) at 12 kHz, and (e) at 17 kHz (CF of the species courtship song).

  5. 5.

    The tuning is also evident in the responsiveness (spikes/syllable) to stimuli of different frequencies at suprathreshold intensities (Fig. 3).

  6. 6.

    In the range of their best frequencies (BF) the fibers tuned to 4–5 and to 10–12 kHz are similar in intensity characteristics and in relationship of latencies to sound intensity, with a linear relationship between responsiveness and latency (Fig. 4). Within a single calling-song verse, the spike response decreases, and the latency increases, from the first to the fourth syllable (Fig. 5). Even at the highest intensities the discharge rate nerver exceeds 350 Hz.

  7. 7.

    The central arborization and projection areas of all the marked fibers are restricted to the ipsilateral half of the prothoracic ganglion. Assuming that fibers marked include those recorded physiologically, it appears that those tuned to 4–5 kHz terminate exclusively in the “crescent-shaped” neuropile, localized and termed the “auditory neuropile” (Figs. 6, 7). Fibers with a peak sensitivity below 2 kHz differ distinctly from the 4–5 kHz group in that they have additional arborizations outside the auditory neuropile (Fig. 8). As yet no unequivocal data are available regarding the spatial arrangement of the fibers with two sensitivity peaks (both 4–5 and 10–12 kHz) and those tuned to 12 kHz or 17 kHz (Fig. 9).

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Abbreviations

BF :

best frequency

CF :

carrier frequency

References

  • Bacon, J.P., Altman, J.S.: A silver intensification method for cobalt filled neurones in wholemount preparations. Brain Res.138, 359–363 (1977)

    Google Scholar 

  • Casaday, G.B., Hoy, R.R.: Auditory interneurons in the cricketTeleogryllus oceanicus: Physiological and antomical properties. J. Comp. Physiol.121, 1–13 (1977)

    Google Scholar 

  • Dambach, M.: Der Vibrationssinn der Grillen. I. Schwellenmessungen an Beinen frei beweglicher Tiere. J. Comp. Physiol.79, 281–304 (1972)

    Google Scholar 

  • Dambach, M., Huber, F.: Perception of substrate vibration in crickets. In: Symposium mechanoreception. Schwartzkopff, J. (ed.). Abh. Rhein.-Westf. Akad. Wiss.53, 263–280 (1974)

  • Dumortier, B.: The physical characteristics of sound emissions in Arthropoda. In: Acoustic behaviour of animals. Busnel, R.G. (ed.), pp. 346–373. Amsterdam, London, New York: Elsevier 1963

    Google Scholar 

  • Eibl, E.: Verlauf des Hörnerven und Projektion der im Hörnerven verlaufenden Fasern im Prothorakalganglion von Grillen mit Hilfe der CoS-Methode. Staatsarbeit Köln (1974)

  • Eibl, E.: Morphologische und neuroanatomische Untersuchungen zur Sinnesorganausstattung der proximalen Tibienabschnitte und ihrer zentralen Projektionen. Dissertation Köln (1976)

  • Eibl, E.: Morphology of the sense organs in the proximal parts of the tibiae ofGryllus campestris L. andGryllus bimaculatus DeGeer (Insecta, Ensifera). Zoomorphologie89, 185–205 (1978)

    Google Scholar 

  • Eibl, E., Huber, F.: Central projections of tibial sensory fibers within the three thoracic ganglia of crickets (G. campestris L.,G. bimaculatus DeGeer). Zoomorphologie92, 1–17 (1979)

    Google Scholar 

  • Elsner, N., Popov, A.V.: Neuroethology of acoustic communication. Adv. Insect Physiol.13, 229–335 (1978)

    Google Scholar 

  • Fielden, A.: Transmission through the last abdominal ganglion of the dragonfly nymph,Anax Imperator. J. Exp. Biol.37, 832–844 (1960)

    Google Scholar 

  • Hill, K.G.: Carrier frequency as a factor in phonotactic behaviour of female crickets (Teleogryllus commodus). J. Comp. Physiol.93, 7–18 (1974)

    Google Scholar 

  • 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 

  • Huber, F.: Insektensprache: Erforschung der Arbeitsweise kleinerer Nervensysteme. Jahrb. Max-Planck-Ges., pp. 55–78 (1978)

  • Kalmring, K., Lewis, B., Eichendorf, A.: The physiological characteristics of the primary sensory neurons of the complex tibial organ ofDecticus verrucivorus L. (Orthoptera, Tettigonioidea). J. Comp. Physiol.127, 109–121 (1978)

    Google Scholar 

  • Kleindienst, H.U., Koch, T.U., Wohlers, D.W.: Analysis of the cricket auditory system by acoustic stimulation using a closed sound field. (in prep.) (1980)

  • 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 

  • Loftus-Hills, J.J., Littlejohn, M.J., Hill, K.G.: Auditory sensitivity of the crickets,Teleogryllus commodus andT. oceanicus. Nature233, 184–185 (1971)

    Google Scholar 

  • Michel, K.: Das Tympanalorgan vonGryllus bimaculatus DeGeer. (Saltatoria, Gryllidae). Z. Morphol. Tiere77, 285–315 (1974)

    Google Scholar 

  • Michelsen, A.: Frequency discrimination in the locust ear by means of four groups of receptor cells. Nature220, 585–586 (1968)

    Google Scholar 

  • Mörchen, A., Rheinlaender, J., Schwartzkopff, J.: Latency shift in insect auditory nerve fibers. Naturwissenschaften65, 565 (1978)

    Google Scholar 

  • Nocke, H.: Physiological aspects of sound communication in crickets (Gryllus campestris L.). J. Comp. Physiol.80, 141–162 (1972)

    Google Scholar 

  • 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 

  • Popov, A.V.: Electrophysiological study of the functional properties of peripheral and central neurons in the auditory system of the locust. Dissertation, Leningrad, 1–231 (1967) (in Russian)

  • Popov, A.V., Shuvalov, V.F., Svetlogorskaja, I.D., Markovich, A.M.: Acoustic behavior and auditory system in insects. In: Symposium Mechanoreception. Schwartzkopff, J. (ed.). Abh. Rhein.-Westf. Akad. Wiss.53, 281–306 (1974)

  • Popov, A.V., Markovich, A.M., Andjan, A.S.: Auditory interneurones in the prothoracic ganglion of the cricket,Gryllus bimaculatus DeGeer. I. The large segmental auditory neuron (LSAN). J. Comp. Physiol.126, 183–192 (1978)

    Google Scholar 

  • Rehbein, H.G.: Experimentell-anatomische Untersuchungen über den Verlauf der Tympanalnervenfasern im Bauchmark von Feldheuschrecken, Laubheuschrecken und Grillen. Verh. Dtsch. Zool. Ges.66, 184–189 (1973)

    Google Scholar 

  • 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 

  • 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 

  • Rheinlaender, J.: Transmission of acoustic information at three neuronal levels in the auditory system ofDecticus verrucivorus. (Tettigoniidae, Orthoptera). J. Comp. Physiol.97, 1–53 (1975)

    Google Scholar 

  • 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 

  • 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 

  • Weber, T.: Vergleich der Lockgesänge von drei Grillenarten im Hinblick auf artspezifisches Erkennen in der Phonotaxis der Weibchen. Verh. Dtsch. Zool. Ges.71, 176 (1978)

    Google Scholar 

  • Wohlers, D.W., Huber, F.: Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L., Gryllus bimaculatus DeGeer). J. Comp. Physiol.127, 11–28 (1978)

    Google Scholar 

  • Wohlers, D.W., Williams, J.L.D., Huber, F., Moore, T.E.: Central projections of fibers in the auditory and tensor nerves of cicadas (Homoptera, Cicadidae). Cell Tissue Res.203, 35–51 (1979)

    Google Scholar 

  • Young, D., Ball, E.: Structure and development of the auditory system in the prothoracic leg of the cricketTeleogryllus commodus (Walker). Z. Zellforsch.147, 293–312 (1974)

    Google Scholar 

  • Zaretsky, M.D., Eibl, E.: Carrier frequency sensitive auditory neurons in crickets and their anatomical projection to the central nervous system. J. Insect Physiol.24, 87–95 (1978)

    Google Scholar 

  • Zhantiev, R.D.: Frequency characteristics of tympanal organs in bushcrickets (Orthoptera, Tettigoniidae). Zool. J.50, 507–514 (1971) (in Russian)

    Google Scholar 

  • Zhantiev, R.D., Korsunovskaja, O.S.: Morphofunctional organization of tympanal organs inTettigonia cantans (Orthoptera, Tettigoniidae). Zool. J.57, 1012–1016 (1978)

    Google Scholar 

  • Zhantiev, R.D., Tshukanov, V.S.: Frequency characteristics of tympanal organs of the cricket,Gryllus bimaculatus DeGeer (Orthoptera, Gryllidae). Vestn. MGU, Ser. Biol.2, 3–8 (1972)

    Google Scholar 

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Author notes

  1. Harald Esch

    Present address: Department of Biology, University of Notre Dame, 46556, Notre Dame, Indiana, USA

Authors and Affiliations

  1. Abteilung Huber, Max-Planck-Institut für Verhaltensphysiologie, D-8131, Seewiesen, Federal Republic of Germany

    Harald Esch, Franz Huber & David W. Wohlers

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  1. Harald Esch
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  2. Franz Huber
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  3. David W. Wohlers
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Supported by the Deutsche Forschungsgemeinschaft as part

Supported by the Deutsche Forschungsgemeinschaft as part

Supported by the Deutsche Forschungsgemeinschaft as part

We are grateful to Dr. U.T. Koch and Dipl. Phys. H.U. Kleindienst for assistance in setting up and calibrating the acoustic stimulator, as well as to Ms. Bamberg for assistance with the figures. We also thank Dr. J. Thorson and H.U. Kleindienst for their critical reading of the manuscript; Dr. Biederman-Thorson kindly translated the original German manuscript into English.

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Esch, H., Huber, F. & Wohlers, D.W. Primary auditory neurons in crickets: Physiology and central projections. J. Comp. Physiol. 137, 27–38 (1980). https://doi.org/10.1007/BF00656914

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