Journal of Comparative Physiology A

, Volume 158, Issue 3, pp 391–404 | Cite as

Interneurones responding to sound in the tobacco budworm mothHeliothis virescens (Noctuidae): morphological and physiological characteristics

  • G. S. Boyan
  • J. H. Fullard
Article

Summary

  1. 1.

    A group of 7 acoustically activated interneurones has been identified in the central nervous system of the noctuid mothHeliothis virescens. The neurones have their cell bodies and major processes in either the mesoor metathoracic neuromeres of the fused pterothoracic ganglion, and axons contralateral to the cell body (Figs. 1, 2). All neurones except one project via the contralateral connective to at least the prothoracic ganglion.

     
  2. 2.

    The frequency-response characteristics and auditory thresholds for most interneurones were similar to that of the A1 receptor (40–45 dB SPL at 16 kHz) (Fig. 3A). Interneurone intensity-response characteristics were also generally of the sigmoid type displayed by the A1 and A2 receptors (Fig. 3B).

     
  3. 3.

    Each interneurone responded to a tone with a compound EPSP of characteristic shape (Figs. 2, 4, 5). In two neurones with very similar responses, the shapes of the rising and plateau phases of their EPSPs, and the suggestion of a delayed input to one neurone, were sufficient to distinguish them (Fig. 5).

     
  4. 4.

    The subthreshold responses of all identified interneurones considerably outlasted the stimulus duration, but spiking patterns reflected stimulus duration more accurately (Figs. 4, 5, 6). Most neurones responded in a tonic or phasic/tonic manner, suggesting they might be ‘repeater’ type neurones; whereas one local (Fig. 2) and one unidentified interneurone (Fig. 9) responded like ‘pulse-coder’ neurones.

     
  5. 5.

    All responses to sound by identified interneurones were excitatory, and no sound-related IPSPs were seen (Figs. 2, 3, 4). Further, little habituation of the response occurred in any interneurone for stimulus rates up to 20/s (Fig. 7A, B).

     
  6. 6.

    The latency of the EPSP from stimulus onset in several interneurones (501, 503, 504) was in each case equivalent to a synaptic delay of less than 1 ms compared with the response latency of the A1 receptor, suggesting direct connectivity (Table 1). The input-output curves and EPSP of neurone 501 changed in such a way as to suggest a possible additional input from the A2 receptor at higher intensities (Figs. 3 B, 4).

     
  7. 7.

    Electrical stimulation of the tympanal nerve and sound stimulation of the ear evoked a similar EPSP and spike pattern in interneurone 502 (Fig. 8A, B). However, the latency of the EPSP in neurone 502 elicited by electrical stimulation was too long (9 ms) for the connection between neurone 502 and either A1 or A2 receptors to be direct.

     
  8. 8.

    The neuronal morphologies and response characteristics described above provided the basis for a simple model of the neural circuitry mediating the phonotactic response of a moth to a bat call (Fig. 10).

     

Abbreviations

CNS

Central nervous system

EPSP

Excitatory postsynaptic potential

IPSP

Inhibitory postsynaptic potential

SPL

Sound pressure level

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References

  1. Agee HR (1967) Response of acoustic sense cell of the bollworm and tobacco budworm to ultrasound. J Econ Entomol 60:366–369Google Scholar
  2. Alonso N, Coro F (1984) Interneuronas auditivas torácicas enEmpyreuma pugione (Lepidoptera: Ctenuchidae). Cien Biol 11:3–15Google Scholar
  3. Altman JS, Shaw MK, Tyrer NM (1980) Input synapses onto a locust sensory neurone revealed by cobalt-electron microscopy. Brain Res 189:245–250Google Scholar
  4. Bentley DR (1969) Intracellular activity in cricket neurons during the generation of behaviour patterns. J Insect Physiol 15:677–699Google Scholar
  5. Boyan GS (1983) Postembryonic development in the auditory system of the locust. Anatomical and physiological characterisation of interneurones ascending to the brain. J Comp Physiol 151:499–513Google Scholar
  6. Boyan GS (1985) Auditory input to the flight system of the locust. J Comp Physiol A 156:79–91Google Scholar
  7. Boyan GS, Altman JS (1985) The suboesophageal ganglion: a ‘missing link’ in the auditory pathway of the locust. J Comp Physiol A 156:413–428Google Scholar
  8. Coro F, Pérez M (1983) Peripheral interaction in the tympanic organ of a moth. Naturwissenschaften 70:99–100Google Scholar
  9. Coro F, Pérez M (1984) Intensity coding by auditory receptors inEmpyreuma pugione (Lepidoptera, Ctenuchidae). J Comp Physiol A 154:287–295Google Scholar
  10. Elepfandt A (1980) Morphology and output coupling of wing muscle motoneurons in the field cricket (Gryllidae, Orthoptera). Zool Jb Physiol 84:26–45Google Scholar
  11. Fielden A (1960) Transmission through the last abdominal ganglion of the dragonfly nymph,Anax imperator. J Exp Biol 37:832–844Google Scholar
  12. Fullard JH (1982) Cephalic influences on a defensive behaviour in the dogbane tiger moth,Cycnia tenera. Physiol Entomol 7:157–162Google Scholar
  13. Fullard JH (1984a) Acoustic relationships between tympanate moths and the Hawaiian hoary bat (Lasiurus cinereus smotus). J Comp Physiol A 155:795–801Google Scholar
  14. Fullard JH (1984b) Listening for bats: pulse repetition rate as a cue for a defensive behaviour inCycnia tenera (Lepidoptera: Arctiidae). J Comp Physiol A 154:249–252Google Scholar
  15. Fullard JH, Barclay RMR (1980) Audition in spring species of arctiid moths as a possible response to differential levels of insectivorous bat predation. Can J Zool 58:1745–1750Google Scholar
  16. Kalmring K (1975) The afferent auditory pathway in the ventral cord ofLocusta migratoria (Acrididae). I. Synaptic connectivity and information processing among the auditory neurons of the ventral cord. J Comp Physiol 104:103–141Google Scholar
  17. Kammer AE (1971) The motor output during turning flight in a hawkmoth,Manduca sexta. J Insect Physiol 17:1073–1086Google Scholar
  18. Kick SA, Simmons JA (1984) Automatic gain control in the bat's sonar receiver and the neuroethology of echolocation. J Neurosci 4:2725–2737Google Scholar
  19. Kondoh Y, Obara Y (1982) Anatomy of motoneurones innervating mesothoracic indirect flight muscles in the silkmoth,Bombyx mori. J Exp Biol 98:23–37Google Scholar
  20. Miller LA (1982) The orientation and evasive behavior of insects to bat cries. In: Addink ADF, Spronk N (eds) Exogenous and endogenous influences on metabolism and neural control, vol. I. Pergamon Press, Oxford, pp 393–405Google Scholar
  21. Miller LA, Olesen J (1979) Avoidance behavior in green lacewings. I. Behavior of free flying green lacewings to hunting bats and ultrasound. J Comp Physiol 131:113–120Google Scholar
  22. Novick A (1977) Acoustic orientation. In: Wimsatt WA (ed) Biology of bats, vol III. Academic Press, New York, pp 73–87Google Scholar
  23. Nüesch H (1957) Die Morphologie des Thorax vonTelea polyphemus (Lepid.). II. Nervensystem. Zool Jahrb 75:615–642Google Scholar
  24. Olesen J, Miller LA (1979) Avoidance behavior in green lacewings. II. Flight muscle activity. J Comp Physiol 131:121–128Google Scholar
  25. Paul DH (1973) Central projections of the tympanic fibres in noctuid moths. J Insect Physiol 19:1785–1792Google Scholar
  26. Paul DH (1974) Responses to acoustic stimulation of thoracic interneurons in noctuid moths. J Insect Physiol 20:2205–2218Google Scholar
  27. Payne RS, Roeder KD, Wallman J (1966) Directional sensitivity of the ears of noctuid months. J Exp Biol 44:17–31Google Scholar
  28. Pearson KG, Boyan GS, Bastiani M, Goodman CS (1985) Heterogeneous properties of segmentally homologous interneurons in the ventral nerve cord of locusts. J Comp Neurol 233:133–145Google Scholar
  29. Pérez M, Coro F (1984) Physiological characteristics of the tympanic organ in noctuid moths. I. Responses to brief acoustic pulses. J Comp Physiol A 154:441–447Google Scholar
  30. Pérez M, Zhantiev RD (1976) Functional organization of the tympanal organ of the flour moth,Ephestia kuehniella. J Insect Physiol 22:1267–1273Google Scholar
  31. Pollack GS, Hoy R (1981) Phonotaxis in flying crickets: neural correlates. J Insect Physiol 27:41–45Google Scholar
  32. Pond CM (1972) The initiation of flight in unrestrained locusts,Schistocerca gregaria. J Comp Physiol 80:163–178Google Scholar
  33. Rehbein HG (1976) Auditory neurons in the ventral cord of the locust: morphological and functional properties. J Comp Physiol 110:233–250Google Scholar
  34. Reichert H, Rowell CHF (1985) Integration of non-phaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218Google Scholar
  35. Rind CF (1983) The organization of flight motoneurones in the moth,Manduca sexta. J Exp Biol 102:239–251Google Scholar
  36. Robertson RM, Pearson KG (1983) Interneurones in the flight system of the locust: distribution, connections, and resetting properties. J Comp Neurol 215:33–50Google Scholar
  37. Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53:110–128Google Scholar
  38. Roeder KD (1964) Aspects of the noctuid tympanic organ having significance in the avoidance of bats. J Insect Physiol 10:529–546Google Scholar
  39. Roeder KD (1965) Moths and ultrasound. Sci Am 212:94–102Google Scholar
  40. Roeder KD (1966) Interneurons of the thoracic nerve cord activated by tympanic nerve fibres in noctuid moths. J Insect Physiol 12:1227–1244Google Scholar
  41. Roeder KD (1967) Turning tendency of moths exposed to ultrasound while in stationary flight. J Insect Physiol 13:873–888Google Scholar
  42. Roeder KD (1969a) Acoustic interneurones in the brain of noctuid moths. J Insect Physiol 15:825–838Google Scholar
  43. Roeder KD (1969b) Brain interneurons in noctuid moths: differential suppression by high sound intensities. J Insect Physiol 15:1713–1718Google Scholar
  44. Roeder KD (1973) Brain interneurons in noctuoid moths: binaural excitation and slow potentials. J Insect Physiol 19:1591–1601Google Scholar
  45. Roeder KD (1974) Responses of the less sensitive acoustic sense cells in the tympanic organs of some noctuid and geometrid moths. J Insect Physiol 20:55–66Google Scholar
  46. Roeder KD (1976) Nerve cells and insect behaviour, revised edn. Harvard University Press, Cambridge, Mass.Google Scholar
  47. Roeder KD, Payne RS (1966) Acoustic orientation of a moth in flight by means of two sense cells. Symp Soc Exp Biol 20:251–272Google Scholar
  48. Roeder KD, Treat AE (1957) Ultrasonic reception by the tympanic organ of noctuid moths. J Exp Zool 134:127–157Google Scholar
  49. Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155:249–262Google Scholar
  50. Römer H, Rheinlaender J (1983) Electrical stimulation of the tympanal nerve as a tool for analysing the responses of auditory interneurons in the locust. J Comp Physiol 152:289–296Google Scholar
  51. Römer H, Seikowski U (1985) Responses to model songs of auditory neurons in the thoracic ganglia and brain of the locust. J Comp Physiol A 156:845–860Google Scholar
  52. Simmons JA, Fenton MB, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 203:16–21Google Scholar
  53. Suga N (1961) Functional organization of two tympanic neurons in noctuid moths. Jpn J Physiol 11:666–677Google Scholar
  54. Surlykke A (1984) Hearing in notodontid moths: a tympanic organ with a single auditory neurone. J Exp Biol 113:323–335Google Scholar
  55. Surlykke A, Miller LA (1982) Central branchings of three sensory axons from a moth ear (Agrotis segetum, Noctuidae). J Insect Physiol 28:356–364Google Scholar
  56. Tomioka K, Yamaguchi T (1984) Response modification of cricket sensory interneurons during flight. Zool Sci 1:169–186Google Scholar
  57. Treat AE (1955) The responses to sound in certain Lepidoptera. Ann Entomol Soc Am 48:272–284Google Scholar
  58. Tyrer NM, Altman JS (1974) Motor and sensory flight neurones in a locust demonstrated using cobalt chloride. J Comp Neurol 157:117–138Google Scholar
  59. Tyrer NM, Gregory GE (1982) A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Phil Trans R Soc Lond B 297:91–123Google Scholar
  60. Watson AHD, Burrows M (1983) The morphology, ultrastructure, and distribution of synapses on an intersegmental interneurone of the locust. J Comp Neurol 214:154–169Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • G. S. Boyan
    • 1
  • J. H. Fullard
    • 2
  1. 1.Department of PhysiologyUniversity of AlbertaEdmontonCanada
  2. 2.Department of BiologyErindale College, University of TorontoMississaugaCanada

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