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Transmission of acoustic information at three neuronal levels in the auditory system ofDecticus verrucivorus (Tettigoniidae, Orthoptera)

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Summary

  1. 1.

    The responses of single acoustic neurons to sound stimuli were recorded by capillary microelectrodes at three sequential stations (the receptors, the ventral cord, and the supraesophageal ganglion) of the auditory pathway of the tettigoniid speciesDecticus verrucivorus.

  2. 2.

    To characterize the responses to sound stimuli varying in intensity, frequency, direction, and duration, the following four basic measures were used: response fields (threshold and constant-response curves vs. frequency), intensity characteristics, directional diagrams, and the time course of the neuronal discharge. These measures are employed to compare both neurons at each station and those at different levels, so that the progressive development of neuronal information processing can be followed from the receptors to the brain.

  3. 3.

    At the receptor level two groups of neurons can be distinguished; on the basis of general morphological comparisons their origins are ascribed to the crista acustica (group a) and the intermediate organ (group b) (Fig. 2).

  4. 4.

    Receptor cells of group a differ among themselves in characteristic frequency and threshold. Bach carries out a precise coding of intensity and direction in its nearthreshold region (Figs. 1, 3, 5 and 6), but with stimuli more than about 30 dB above threshold, the response saturates. The response areas of different cells overlap so that, taken as a whole, they ensure relatively precise transduction of the above-mentioned stimulus parameters over a wide range of frequencies and intensities.

  5. 5.

    Group-b receptor cells (intermediate organ) are considerably less sensitive to changes in stimulus frequency, intensity, and direction (Figs. 2 and 10). Like those of group a they respond nearly tonically to stimuli sufficiently above threshold (Figs. 7 and 11), though with long stimuli a slight initial phasic component is discernible (Fig. 8).

  6. 6.

    The neurons of the ventral cord receive synaptic input from several tympanic units of the same side, and in many cases informations of the opposite side as well. The observed unilateral and bilateral effects can be brought about by facilitation and inhibition. As a result of this complex integration the discrimination of certain sound parameters available in the receptor-cell responses can, at the ventral-cord level, either be enhanced considerably or be degraded.

  7. 7.

    Whereas frequency selectivity at the higher levels is severely degraded in comparison with that available at the receptor level (Figs. 13, 14, 15 and 29), the precision of intensity and direction coding is distinctly enhanced (Figs. 17, 18, 30 and 31). The response patterns recorded inchide those of phasic units, tonic units, and intermediate forms, as well as units which alter the pattern with stimulus conditions. Several of these are well matched to specific features of the stridulation sounds of the species (Figs. 20 and 21).

  8. 8.

    As far as the processing of frequency and intensity is concerned, only quantitative differences—no fundamental or qualitative differences—were observed in comparisons of the ventral cord and the supraesophageal ganglion (Figs. 24 and 26). With respect to the coding of direction and form of the response pattern, however, characteristic novel units are found in the supraesophageal ganglion (Figs. 25, 27, 28 and 33). Finally, the extent to which “recognition filters” exist at the level of the ventral cord and the supraesophageal ganglion is discussed in terms of the known aspects of acoustic behavior.

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References

  • Adam, L.-J.: Neurophysiologie des Hörens und Bioakustik einer Feldheuschrecke (Locusta migratoria). Z. vergl. Physiol.63, 227–289 (1969)

    Google Scholar 

  • Adam, L.-J.: Die Darstellung der akustischen Reizsituation im Gehirn der Wanderheuschrecke. Verh. dtsch. zool. Ges.66, 176–184 (1972)

    Google Scholar 

  • Adam, L.-J., Schwartzkopff, J.: Getrennte nervöse Repräsentation für verschiedene Tonbereiche im Protocerebrum vonLocusta migratoria. Z. vergl. Physiol.54, 246–255 (1967)

    Google Scholar 

  • Alexander, R. D.: Sound communication in Orthoptera and Cicadidae. In: Animal sounds and communication, ed. Lanyon and Tavolga. Symp. Amer. Inst. Biol. Sci.7, 38–92 1960

  • Autrum, H.: Über Lautäußerung und Schallwahrnehmung bei Arthropoden II. Das Richtungshörenvon Locusta und Versuch einer Hörtheorie für Tympanalorgane vom Locustidentyp. Z. vergl. Physiol.28, 326–352 (1940)

    Google Scholar 

  • Autrum, H.: Über Gehör- und Erschütterungssinn bei Locustiden. Z. vergl. Physiol.28, 580–637 (1941)

    Google Scholar 

  • Autrum, H.: Über kleinste Reize bei Sinnesorganen. Biol. Zbl.63, 209–236 (1943)

    Google Scholar 

  • Autrum, H.: Phasische und tonische Antworten vom Tympanalorgan vonTettigonia viridissima. Acustica10, 339–348 (1960)

    Google Scholar 

  • Autrum, H., Schwartzkopff, J., Swoboda, H.: Der Einfluß der Schallrichtung auf die Tympanal-Potentiale vonLocusta migratoria. Biol. Zbl.80, 385–402 (1961)

    Google Scholar 

  • Burrows, M., Rowell, C. H. F.: Connections between descending visual interneurons and metathoracic motoneurons in the locust. J. comp. Physiol.85, 221–234 (1973)

    Google Scholar 

  • Busnel, M.-C.: Contribution a l'étude des émissions acoustiques des Orthoptères. Ann. I.N.R.A.3, 333–421 (1953)

    Google Scholar 

  • Busnel, M.-C., Dumortier, B., Busnel, R.-G.: Recherche sur la phonocinèse de certains insectes. Bull. Soc. Zool. Fr.84, 351–370 (1959)

    Google Scholar 

  • Cook, P. M.: Observations on giant fibres of the nervous system ofLocusta migratoria. Quart. J. micr. Sci.92, 297–305 (1951)

    Google Scholar 

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

    Google Scholar 

  • Dambach, M.: Der Vibrationssinn bei Grillen. II. Antworten von Neuronen im Bauchmark. J. comp. Physiol.79, 305–324 (1972)

    Google Scholar 

  • Dörrscheidt, G. J.: Statistical modulation analysis of animal sounds as a basis for computer synthesised quasinatural stimuli in bioacoustical research. Proceedings of the 2nd Seminar on Experimental Simulation and Solving of Probability Problems. Prag, p. 32–51. 1973

  • Dubrovin, N. N., Zhantiev, R. D.: Acoustic signals of katydids (Orthoptera, Tettigoniidae) [in Russian]. Zool. Zh. (Moscow)49, 1001–1014 (1970)

    Google Scholar 

  • Dumortier, B.: The physical characteristics of sound emissions in Arthropoda. In: Acoustic behaviour of animals, ed. R.-G. Busnel. Amsterdam: Elsevier Publ. Co. 1963

    Google Scholar 

  • Eisner, N., Huber, F.: Neurale Grundlage artspezifischer Kommunikation bei Orthopteren. Portschr. Zool.22, 1–48 (1973)

    Google Scholar 

  • Gray, E. G.: The fine structure of the insect ear. Phil. Trans.B 243, 75–94 (1960)

    Google Scholar 

  • Heiversen, D. von: Gesang des Männchens und Lautschema des Weibchens bei der FeldheuschreckeChorthippus biguttulus (Orthoptera, Acrididae). J. comp. Physiol.81, 381–422 (1972)

    Google Scholar 

  • Horridge, G. A.: Pitch discrimination in Orthoptera (Insecta) demonstrated by responses of central auditory neurons. Nature (Lond.)185, 623–624 (1960)

    Google Scholar 

  • Howse, P. E., Lewis, D. B., Pye, J. D.: Adequate stimulus of the insect tympanic organ. Experientia (Basel)27, 598–600 (1971)

    Google Scholar 

  • Johnstone, B. M., Saunders, J. C., Johnstone, J. R.: Tympanic membrane response in the cricket. Nature (Lond.)227, 625–626 (1970)

    Google Scholar 

  • Kalmring, K.: Akustische Neuronen im Unterschlundganglion der WanderheuschreckeLocusta migratoria. Z. vergl. Physiol.72, 95–110 (1971)

    Google Scholar 

  • Kalmring, K., Rheinlaender, J., Rehbein, H. G.: Akustische Neuronen im Bauchmark der WanderheuschreckeLocusta migratoria. Z. vergl. Physiol.76, 314–332 (1972)

    Google Scholar 

  • Kalmring, K., Rheinlaender, J., Römer, H.: Akustische Neuronen im Bauchmark vonLocusta migratoria. Der Einfluß der Schallrichtung auf die Antwortmuster. J. comp. Physiol.80, 325–352 (1972)

    Google Scholar 

  • Katsuki, Y.: Neural mechanisms of hearing in cats and insects. In: Electrical activity of single cells, ed. Y. Katsuki. Tokyo: Igakushoin, Hongo 1960

    Google Scholar 

  • Katsuki, Y., Suga, N.: Electrophysiological studies on hearing in common insects in Japan. Proc. Jap. Acad.34, 633–638 (1958)

    Google Scholar 

  • Katsuki, Y., Suga, N.: Neural mechanism of hearing in insects. J. exp. Biol.37, 279–290 (1960)

    Google Scholar 

  • Loher, W.: Untersuchungen über den Aufbau und die Entstehung der Gesänge einiger Feldheuschreckenarten und den Einfluß von Lautzeichen auf das akustische Verhalten. Z. vergl. Physiol.39, 313–356 (1957)

    Google Scholar 

  • McKay, J. M.: The auditory system ofHomorocoryphus (Tettigoniidae, Orthoptera). J. exp. Biol.51, 787–802 (1969)

    Google Scholar 

  • McKay, J. M.: Central control of an insect sensory interneurone. J. exp. Biol.53, 137–145 (1970)

    Google Scholar 

  • Michelsen, A.: Pitch discrimination in the locust ear: Observations on single cells. J. Insect Physiol.12, 1119–1131 (1966)

    Google Scholar 

  • Michelsen, A.: The physiology of the locust ear. I. Frequency sensitivity of single cells in the isolated ear. II. Frequency discrimination based upon resonances in the tympanum. III. Acoustical properties of the intact ear. Z. vergl. Physiol.71, 49–128 (1971)

    Google Scholar 

  • Morse, Ph. M., Rubenstein, P. J.: The diffraction of waves by ribbons and by slits. Physic. Rev.54, 895–898 (1938)

    Google Scholar 

  • Murphey, R. K., Zaretsky, D. D.: Orientation to calling song by female crickets,Scapsipedus marginatus (Gryllidae). J. exp. Biol.56, 335–352 (1972)

    Google Scholar 

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

    Google Scholar 

  • Perkelm, D. H., Gerstein, G. L., Moore, G. P.: Neuronal spike trains and stochastic point processes. I. The single spike train. Biophys. J.7, 391–418 (1967)

    Google Scholar 

  • Popov, A. V.: Electrophysiological studies on peripheral auditory neurons in the locust [in Russian]. J. evol. biochem. Physiol.1, 239–250 (1965)

    Google Scholar 

  • Popov, A. V.: Comparative analysis of sound signals and some principles of auditory system organization in cicadas and orthoptera [in Russian]. In: Modern problems of structure and function of the nervous system of insects. Leningrad: Nauka 1969

    Google Scholar 

  • Popov, A. V.: Frequency selectivity of the reaction of auditory neurons in the 1st thoracic ganglion of the cricketGryllus bimaculatus. J. evol. biochem. Physiol.9, 265–277 (1973)

    Google Scholar 

  • Popov, A. V., Svetlogorskaya, I. D.: Ultrastructural organization of the auditory nerve in the locustLocusta migratoria (on the problem of interaction between the receptors). J. evol. biochem. Physiol.7, 516–521 (1971)

    Google Scholar 

  • Regen, J.: Über die Anlockung des Weibchens vonQryllus campestris L. durch die telefonisch übertragenen Stridulationslaute des Männchens. Ein Beitrag zur Frage der Orientierung bei den Insekten. Pflügers Arch. Ges. Physiol.155, 193–200 (1913)

    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 (1972)

    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., Kalmring, K.: Die afferente Hörbahn in Bereich des Zentralnervensystems vonDecticus verrucivorus (Tettigoniidae). J. comp. Physiol.85, 361–410 (1973)

    Google Scholar 

  • Rheinlaender, J., Kalmring, K., Römer, H.: Akustische Neuronen mit T-Struktur im Bauchmark von Tettigoniiden. J. comp. Physiol.77, 208–224 (1972)

    Google Scholar 

  • Rheinlaender, J., Schwartzkopff, J.: Verarbeitung von Frequenz und Intensität in der Hörbahn von Laubheuschrecken. Naturwissenschaften61, 366–367 (1974)

    Google Scholar 

  • Roeder, K. D.: Interneurons of the thoracic nerve cord activated by tympanic nerve fibres in noctuid moths. J. Insect Physiol.12, 1227–1244 (1966)

    Google Scholar 

  • Roeder, K. D.: Acoustic interneurons in the brain of noctuid moths. J. Insect Physiol.15, 825–838 (1969)

    Google Scholar 

  • Roeder, K. D.: Responses of the less sensitive acoustic sense cells in the tympanic organs of some noctuid and geometrid moths. J. Insect Physiol.20, 55–66 (1974)

    Google Scholar 

  • Roeder, K. D., Treat, E. A.: Ultrasonic reception by the tympanic organ of noctuid moths. J. exp. Zool.134, 127–158 (1957)

    Google Scholar 

  • Roeder, K. D., Treat, E. A.: The reception of bat cries by the tympanic organ of noctuid moths. In: Sensory communication, ed. W. Rosenblith. New York: M.I.T. Press 1961

    Google Scholar 

  • Römer, H.: Statistische Analyse der Antwortmuster zur Identifizierung von akustischen Sekundärneuronen im Bauchmark der LaubheuschreckeTettigonia viridissima. Diplomarbeit Bochum, 1973

  • Rowell, C. H. F., McKay, J. M.: An acridid auditory interneurone. I. Functional connexions and response to single sounds. J. exp. Biol.51, 231–245 (1969)

    Google Scholar 

  • Schlue, W. R.: Zur zentralnervösen Organisation des Cereal-Flucht-Reflexes der Schabe. Z. Tierpsych.34, 172–207 (1974)

    Google Scholar 

  • Schwabe, J.: Beiträge zur Morphologie und Histologie der tympanalen Sinnesapparate der Orthopteren. Zoologica (Stuttg.)50, 1–154 (1906)

    Google Scholar 

  • Schwartzkopff, J.: Neue Ergebnisse zur Informationsaufnahme und Informationsverarbeitung in Sinnesorganen. Nova Acta Leopold.37 (2), 232–239 (1973)

    Google Scholar 

  • Schwartzkopff, J.: Principles of signal detection by the auditory pathway of invertebrates and vertebrates. In: Mechanoreception, ed. J. Schwartzkopff, Symp. Bochum 1973. Wiss. Abh. Rhein.-Westf. Akad. Wiss., in press (1974)

  • Schumacher, R.: Morphologische Untersuchungen der tibialen Tympanalorgane von neun einheimischen Laubheuschreckenarten (Orthoptera, Tettigonioidea). Z. Morph. Tiere75, 267–282 (1973)

    Google Scholar 

  • Strutt, M. J. O.: Beugung einer ebenen Welle an einem Spalt von endlicher Breite. Z. Physik69, 597–617 (1931)

    Google Scholar 

  • Suga, N.: Peripheral mechanism of hearing in locust. Jap. J. Physiol.10, 533–546 (1960)

    Google Scholar 

  • Suga, N.: Functional organization of two tympanic neurons in noctuid moths. Jap. J. Physiol.11, 666–677 (1961)

    Google Scholar 

  • Suga, N.: Central mechanism of hearing and sound localization in insects. J. Insect Physiol.9, 867–873 (1963)

    Google Scholar 

  • Suga, N.: Ultrasonic production and its reception in some neotropical Tettigoniidae. J. Insect Physiol.12, 1039–1050 (1966)

    Google Scholar 

  • Suga, N., Katsuki, Y.: Central mechanism of hearing in insects. J. exp. Biol.38, 545–558 (1961).

    Google Scholar 

  • Suga, N., Katsuki, Y.: Pharmacological studies on the auditory synapses in a grasshopper. J. exp. Biol.38, 759–770 (1961)

    Google Scholar 

  • Zhantiev, R. D.: Frequency Charakteristik of tympanal organs in grasshoppers (Orthoptera, Tettigoniidae [in Russian]. Zool. Zh. (Moscow)50, 507–514 (1971)

    Google Scholar 

  • Zhantiev, R. D., Dubrovin, N. N.: Directional sensitivity of auditory organs in katydids (Orthoptera, Tettigoniidae) [in Russian]. In: Adaptive mechanisms of acoustic orientation, Moscow University 1973

  • Zhantiev, R. D., Tshukanov, V. S.: Frequency characteristics of tympanal organs of the cricketGryllus bimaculatus Deg. (Orthoptera, Gryllidae) [in Russian]. Vestn. Mosk. Univ.2, 3–8 (1972)

    Google Scholar 

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  1. Lehrstuhl für Allgemeine Zoologie der Ruhr-Universität Bochum, Bochum, Germany

    Jürgen Rheinlaender

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  1. Jürgen Rheinlaender
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Supported by Deutsche Forschungsgemeinschaft, grants to J. Schwartzkopff and SFB 114.

I gratefully acknowledge the assistance of Dr. K. Kalmring and the helpful criticism of Prof. Dr. J. Schwartzkopff. I thank Dr. H.-J. Leppelsack for making the computer program available to me. Dr. M. A. Biederman-Thorson was so kind as to translate the German manuscript and Mrs. Ch. Klotz to type it.

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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). https://doi.org/10.1007/BF00635647

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