Journal of comparative physiology

, Volume 152, Issue 2, pp 155–167 | Cite as

Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior

  • Andrew Moiseff
  • Ronald Hoy


  1. 1.

    In the cricket,Teleogryllus oceanicns, an identified auditory interneuron, interneuron-1 (int-1), is described morphologically and physiologically (Figs. 1,2). There is one such neuron in each hemiganglion of the prothoracic ganglion. The medial dendrites of int-1 overlap part of the terminal field formed by the auditory afferent axons from the ear and int-1's axon ascends to the brain, terminating on the same (ipsilateral) side (Fig- 2).

  2. 2.

    The neuron has a two-part frequency response characteristic: (1) its spontaneous activity is suppressed by low frequencies (3 to 8 kHz) at threshold-to-moderate intensities (Fig. 9 B), and (2) it is strongly excited at high frequencies, especially ultrasonic, from 15–100 kHz (Fig. 3).

  3. 3.

    Int-1 produces more spikes per tone pulse (Fig. 4) and its reponse latency decreases (Fig. 5), with increasing levels of intensity when stimulated by ultrasound.

  4. 4.

    Two-tone inhibition occurs in int-1. When a 30 kHz (normally excitatory) tone is combined with a 5 kHz tone (which suppresses spontaneous activity), the combination tone results in a diminished response, compared to the response to the excitatory tone alone (Fig. 6).

  5. 5.

    The excitation of int-1 shows lateralization. Excitation is stronger in the neuron ipsilateral to the sound source, than in the contralateral int-1 (Fig. 9).

  6. 6.

    Int-1 responds to electronically-generated pulse trains that simulate bat-echolocation signals. The neuron is responsive to a range of ultrasonic frequencies that are contained in the echolocation signals of insectivorous bats (Fig. 11).

  7. 7.

    In light of its response characteristics, we speculate that int-1 plays a role in the detection of ultrasonic signals emitted in the cricket's normal environment by hunting bats.



Spontaneous Activity Frequency Response Characteristic Ultrasonic Signal Tone Pulse Afferent Axon 







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  1. Alexander RD (1967) Acoustical communication in arthropods. Annu Rev Entomol 12:495–526Google Scholar
  2. Boyan GS (1981) Two-tone suppression of an auditory neuron in the brain of the cricket: proposed role in phonotactic behavior. J Comp Physiol 144:117–126Google Scholar
  3. Boyan GS, Williams JLD (1982) Auditory neurons in the brain of the cricketGryllus bimaculatus (DeGeer): ascending interneurones. J Insect Physiol 28:493–502Google Scholar
  4. Casaday GB, Hoy RR (1977) Auditory interneurons in the cricketTeleogryllus oceanicus: Physiological and anatomical properties. J Comp Physiol 121:1–13Google Scholar
  5. Eibl E, Huber F (1979) Central projections of tibial sensory fibers within the three thoracic ganglia of crickets. Zoomorphology 92:1–17Google Scholar
  6. Esch H, Huber F, Wohlers D (1980) Physiological and anatomical properties of sensory auditory fibers in crickets,Gryllus bimaculatus DeGeer,Gryllus campestris L. J Comp Physiol 137:27–38Google Scholar
  7. Elsner N, Popov AV (1978) Neuroethology of acoustic communication. Adv Insect Physiol 13:229–355Google Scholar
  8. Griffin DR (1974) Listening in the dark. Dover, New YorkGoogle Scholar
  9. Hill KG (1974) Carrier frequency as a factor in the phonotactic behavior of female crickets (Teleogryllus commodus). J Comp Physio 193:7–18Google Scholar
  10. Hill KG, Loftus-Hills JJ, Gartside DF (1972) Pre-mating isolation between the Australian field cricketsTeleogryllus commodus andT. oceaniens (Orthoptera: Gryllidae). Aust J Zoo 120:153–163Google Scholar
  11. Hoy RR (1978) Acoustic communication in crickets: a model system for the study of feature detection. Fed Proc 37:2316–2323Google Scholar
  12. Hoy RR, Casaday GC (1976) Physiological and anatomical properties of cricket auditory interneurons. Soc Neurosci Abstr 2:347Google Scholar
  13. Hoy RR, Paul RC (1973) Genetic control of song specificity in crickets. Science 180:82–83Google Scholar
  14. Hoy RR, Rollins S, Casaday G (1978) Absence of auditory afferents alters the growth pattern of an identified auditory interneuron. Soc Neurosci Abstr 4Google Scholar
  15. Huber F (1962) Central nervous control of sound production in crickets and some speculations on its evolution. Evolution 16:429–442Google Scholar
  16. Huber F (1963) The role of the central nervous system in Orthoptera during the co-ordination and control of stridulation. In: Busnel RD (ed) Acoustic behavior of animals. Elsevier, Amsterdam, pp 440–488Google Scholar
  17. Huber F (1975) Sensory and neuronal mechanisms underlying acoustic communication in orthopteran insects. In: Galun R, Hillman P, Parnis I, Werman R (eds) Sensory physiology and behavior. Plenum, New York, pp 55–97Google Scholar
  18. Huber F (1978) The insect nervous system and insect behavior. Anim Behav 26:969–981Google Scholar
  19. Iles JF, Mulloney B (1971) Procion yellow staining of cockroach motorneurons without the use of microelectrodes. Brain Res 30:397–400Google Scholar
  20. Kalmring K (1975) The afferent auditory pathway in the ventral nerve cord ofLocusta migratoria (Acrididae). J Comp Physiol 104:103–141Google Scholar
  21. Kien J (1976) A preliminary report on cobalt sulfide staining of locust visual interneurons through extracellular electrodes. Brain Res 109:158–164Google Scholar
  22. Miller LA (1975) The behavior of flying green lacewings,Chrysopa camea, in the presence of ultrasound. J Insect Physiol 21:205–219Google Scholar
  23. Moiseff A (1980) Auditory interneurons and phonotactic behavior in the Australian field cricket,Teleogryllus oceaniens. PhD dissertation, Cornell University, Ithaca (New York)Google Scholar
  24. Moiseff A, Hoy RR (1979) Frequency dependent response properties of an identified interneuron in the cricketTeleogryllus oceaniens. Soc Neurosci Abstr 4:255Google Scholar
  25. Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056Google Scholar
  26. Oldfield BP (1980) Accuracy of orientation in female crickets,Teleogryllus oceaniens (Gryllidae): dependence on song spectrum. J Comp Physiol 141:93–99Google Scholar
  27. Pitman RM, Tweedle CD, Cohen MJ (1972) Branching of central neurons, intracellular cobalt injection for light and electron microscopy. Science 176:412–414Google Scholar
  28. Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432Google Scholar
  29. Pollack GS, Hoy RR (1981) Phonotaxis in flying crickets: neural correlates. J Insect Physiol 27:41–45Google Scholar
  30. Popov AV, Markovich AM (1982) Auditory interneurones in the prothoracic ganglion of the cricket,Gryllus bimaculatus II. A high-frequency ascending neurone (HF1AN). J Comp Physiol 146:351–359Google Scholar
  31. Popov AV, Shuvalov VF (1977) Phonotactic behavior of crickets. J Comp Physiol 119:111–126Google Scholar
  32. Popov AV, Markovich AM, Andjan AS (1978) Auditory interneurons in the prothoracic ganglion of the cricket,Gryllus bimaculatus deGeer. J Comp Physiol 126:183–192Google Scholar
  33. Popov AV, Shuvalov VF, Markovich AM (1975) Spectrum of the calling songs, phonotaxis and the auditory system in the cricketGryllus bimaculatus. J Evol Biochem Physiol 2:453–460Google Scholar
  34. Regen J (1913) Über die Anlockung des Weibchens vonGryllus campestris L. durch telephonisch übertragene Stridulationslaute des Männchens. Pflügers Arch 155:193–200Google Scholar
  35. Rehbein H, Kalmring K, Römer H (1974) Structure and function of acoustic neurons in the thoracic ventral nerve cord ofLocusta migratoria (Acrididae). J Comp Physiol 95:263–280Google Scholar
  36. Rheinlaender J, Kalmring K, Popov AV, Rehbein H (1976) Brain projections and information processing of biologically significant sounds by two large ventral-cord neurons ofGryllus bimaculatus DeGeer. J Comp Physiol 110:251–269Google Scholar
  37. Roeder KD (1967) Nerve cells and insect behavior. Harvard University Press, CambridgeGoogle Scholar
  38. Sachs M, Kiang N (1968) Two-tone inhibition in auditory nerve fibers. J Acoust Soc Am 43:1120–1128Google Scholar
  39. Shuvalov VF, Popov AV (1971) Reaction of flying females of the domestic cricket,Acheta domesticus to sound signals and its changes in ontogenesis. J Evol Physiol Biochem 7:612–616Google Scholar
  40. Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759Google Scholar
  41. Suga N (1968) Neural responses to sound in a Brazilian mole cricket. J Audit Res 8:129–134Google Scholar
  42. Thorson J, Weber T,- Huber F (1982) Auditory behavior of the cricket. II. Simplicity of the calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378Google Scholar
  43. Tyrer NM, Bell EM (1974) The intensification of cobalt-filled profiles using a modification of Timm's sulfide-silver method. Brain Res 73:151–155Google Scholar
  44. Ulagaraj SM, Walker TJ (1973) Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182:1278–1279Google Scholar
  45. Walker TJ (1957) Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthinae) to calling songs of the males. Ann Entomol Soc Am 50:626–636Google Scholar
  46. Weber T, Thorson J, Huber F (1981) Auditory behavior of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J Comp Physiol 141:215–232Google Scholar
  47. Wohlers DW, Huber F (1978) Intracellular recording and staining of cricket auditory interneurons. J Comp Physiol 127:11–28Google Scholar
  48. Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket,Gryllus bimaculatus L. J Comp Physiol 146:161–173Google Scholar
  49. Zaretsky MD (1972) Specificity of the calling song and short term changes in the phonotactic response by female crickets (Scapsipedus marginatus) (Gryllidae). J Comp Physiol 79:153–172Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • Andrew Moiseff
    • 1
  • Ronald Hoy
    • 1
  1. 1.Section of Neurobiology and BehaviorCornell UniversityIthacaUSA

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