Skip to main content
Log in

Response properties of prothoracic, interganglionic, sound-activated interneurons in the cricketTeleogryllus oceanicus

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

  1. 1.

    The response properties of nine prothoracic interneurons in the cricketTeleogryllus oceanicus are described. Two of these (DN1 and TN1) have been studied previously in another species (Wohlers and Huber 1982); the remaining seven are described here for the first time. Four of the neurons (DN1–DN4) have an axon that projects out of the prothoracic ganglion posteriorly, while the others (TN1–TN5) have axons that project posteriorly and anteriorly.

  2. 2.

    None of the interneurons are sharply tuned, but all show some frequency selectivity. Five are best excited by high frequency tones and show maximum responsiveness in the range 18–40 kHz (Fig. 1). The others are primarily responsive to low frequency tones in the range 3–12 kHz (Fig. 1). All nine neurons receive auditory input in the prothoracic ganglion (Figs. 2–10).

  3. 3.

    Each of the interneurons is direction-sensitive; TN2, TN3 and TN5 are most sensitive to sound played from the soma-ipsilateral side while the others are most sensitive to sound from the soma-contralateral side (Figs. 2–10).

  4. 4.

    Four of the interneurons are able to encode at least some of the temporal features of a model calling song (Fig. 11, Table 1). Only one, however, has a maintained response to continual stimulation; the rest exhibit severely decrementing responses (Fig. 12, Table 1).

  5. 5.

    In addition to responding to sound, some of the neurons respond to wind and/or light (Figs. 2–10).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

EPSP :

excitatory postsynaptic potential

IPSP :

inhibitory postsynaptic potential

PST :

peri-stimulus time

RDI :

response decrement index

References

  • Alexander RD (1960) Sound communication in Orthoptera and Cicadidae. In: Lanyon WE, Tavolga WN (eds) Animal sounds and communication. American Institute of Biological Sciences, Washington DC, pp 38–92

    Google Scholar 

  • Alexander RD (1961) Aggressiveness, territoriality and sexual behavior in field crickets (Orthoptera: Gryllidae). Behaviour 17:130–223

    Google Scholar 

  • Aréchiga H, Wiersma CAG (1969) The effect of motor activity on the reactivity of single visual units in the crayfish. J Neurobiol 1:53–69

    Google Scholar 

  • Atkins G, Pollack GS (1987) Correlations between structure, topographic arrangement, and spectral sensitivity of soundsensitive interneurons in crickets. J Comp Neurol (in press)

  • Atkins G, Ligman S, Burghardt F, Stout JF (1984) Changes in phonotaxis by the female cricketAcheta domesticus L. after killing identified acoustic interneurons. J Comp Physiol A 154:795–804

    Google Scholar 

  • Bentley DR, Hoy RR (1970) Postembryonic development of adult motor patterns in crickets: a neural analysis. Science 170:1409–1411

    Google Scholar 

  • Boyan GS (1980) Auditory neurones in the brain of the cricketGryllus bimaculatus (De Geer). J Comp Physiol 140:81–93

    Google Scholar 

  • Boyan GS (1985) Response decrement in an auditory neurone of the locust. J Insect Physiol 31:99–107

    Google Scholar 

  • Boyan GS, Williams JLD (1981) Descending interneurones in the brain of the cricket. Anatomy and responses to auditory stimuli. Naturwissenschaften 67:486–487

    Google Scholar 

  • Cade WH (1981) Field cricket spacing, and the phonotaxis of crickets and parasitoid flies to clumped and isolated cricket songs. Z Tierpsychol 55:365–375

    Google Scholar 

  • Campbell DJ, Shipp E (1979) Regulation of spatial pattern in populations of the field cricketTeleogryllus commodus (Walker). Z Tierpsychol 51:260–268

    Google Scholar 

  • Casaday GB, Hoy RR (1977) Auditory interneurons in the cricketTeleogryllus oceanicus: physiological and anatomical properties. J Comp Physiol 121:1–13

    Google Scholar 

  • Daley DL, Delcomyn F (1980a) Modulation of the excitability of cockroach giant interneurons during walking. I. Simultaneous excitation and inhibition. J Comp Physiol 138:231–239

    Google Scholar 

  • Daley DL, Delcomyn F (1980b) Modulation of the excitability of cockroach giant interneurons during walking. II. Central and peripheral components. J Comp Physiol 138:241–251

    Google Scholar 

  • Doolan JM, Pollack GS (1985) Phonotactic specificity of the cricketTeleogryllus oceanicus: intensity-dependent selectivity for temporal parameters of the stimulus. J Comp Physiol A 157:223–233

    Google Scholar 

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

    Google Scholar 

  • Furukawa N, Tomioka K, Yamaguchi T (1983) Functional anatomy of the musculature and innervation of the neck and thorax in the cricket,Gryllus bimaculatus. Zool Mag 92:371–385

    Google Scholar 

  • Hedwig B (1986) On the role in stridulation of plurisegmental interneurons of the acridid grasshopperOmocestus viridulus L. II. Anatomy and physiology of ascending and T-shaped interneurons. J Comp Physiol A 158:429–444

    Google Scholar 

  • Hill KG, Loftus-Hills JJ, Gartside DF (1972) Premating isolation between the Australian field cricketsTeleogryllus commodus andT. oceanicus (Orthoptera: Gryllidae). Aust J Zool 20:153–163

    Google Scholar 

  • Horner M, Gras H (1985) Physiological properties of some descending neurons in the cricket brain. Naturwissenschaften 72:603–604

    Google Scholar 

  • Hutchings M, Lewis B (1984) The role of two-tone suppression in song-coding by ventral cord neurones in the cricketTeleogryllus oceanicus (Le Guillou). J Comp Physiol A 154:103–112

    Google Scholar 

  • Kalmring K (1975) The afferent pathway in the ventral cord ofLocusta migratoria (Acrididae). I. Synaptic connectivity and information processing among the auditory neurons of the ventral nerve cord. J Comp Physiol 104:103–141

    Google Scholar 

  • Kühne R, Silver S, Lewis B (1984) Processing of vibratory and acoustic signals by ventral cord neurones in the cricketGryllus campestris. J Insect Physiol 30:575–585

    Google Scholar 

  • Leroy Y (1964) Transmission du parametre fréquence dans les signaux acoustiques des hybrides F1 et P × F1 de deux grillons:Teleogryllus commodus Walker etT. oceanicus Le Guillou (Orthoptères, Ensifères). CR Acad Sci (D) (Paris) 259:892–895

    Google Scholar 

  • Loher W, Rence B (1978) The mating behaviour ofTeleogryllus oceanicus (Walker) and its central and peripheral control. Z Tierpsychol 46:225–259

    Google Scholar 

  • Moiseff A, Hoy R (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior. J Comp Physiol 152:155–167

    Google Scholar 

  • 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 75:4052–4056

    Google Scholar 

  • Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992–994

    Google Scholar 

  • Nolen TG, Hoy RR (1986) Phonotaxis in flying crickets. 1. Attraction to the calling song and avoidance of bat-like ultrasound are discrete behaviors. J Comp Physiol A 159:423–439

    Google Scholar 

  • Oldfield BP, Hill KG (1983) The physiology of ascending auditory interneurons in the tettigoniidCaedicia simplex (Orthoptera: Ensifera): response properties and a model of integration in the afferent auditory pathway. J Comp Physiol 152:495–508

    Google Scholar 

  • Oldfield BP, Kleindienst HU, Huber F (1986) Physiology and tonotopic organization of auditory receptors in the cricketGryllus bimaculatus DeGeer. J Comp Physiol A 159:457–464

    Google Scholar 

  • Orida N, Josephson RK (1978) Peripheral control of responsiveness to auditory stimuli in giant fibers of crickets and cockroaches. J Exp Biol 72:153–164

    Google Scholar 

  • Pollack GS (1984) Ultrasound-sensitive neurons descending in the thoracic nervous system of the cricketTeleogryllus oceanicus. Can J Zool 62:555–562

    Google Scholar 

  • Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432

    Google Scholar 

  • Pollack GS, Hoy RR (1981a) Phonotaxis to individual rhythmic components of a complex cricket calling song. J Comp Physiol 144:367–373

    Google Scholar 

  • Pollack GS, Hoy RR (1981b) Phonotaxis in flying crickets: neural correlates. J Insect Physiol 27:41–45

    Google Scholar 

  • Pollack GS, Plourde N (1982) Directionality of acoustic orientation in flying crickets. J Comp Physiol 146:207–215

    Google Scholar 

  • Popov AV, Markovich AM (1982) Auditory interneurons in the prothoracic ganglion of the cricket,Gryllus bimaculatus. II. A high-frequency ascending neurone (HF1AN). J Comp Physiol 146:351–359

    Google Scholar 

  • Popov AV, Markovich AM, Andjan AS (1978) Auditory interneurons in the prothoracic ganglion of the cricket,Gryllus bimaculatus deGeer. I. The large segmental auditory neuron (LSAN). J Comp Physiol 126:183–192

    Google Scholar 

  • Regen J (1914) Über die Anlockung des Weibchens vonGryllus campestris L. durch telephonisch übertragene Stridulationslaute des Männchens. Ein Beitrag zur Frage der Orientierung bei den Insekten. Pfügers Arch Ges Physiol 155:193–200

    Google Scholar 

  • Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J Neurophysiol 53:1201–1218

    Google Scholar 

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

    Google Scholar 

  • Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79

    Google Scholar 

  • Schmitz B, Scharstein H, Wendler G (1983) Phonotaxis inGryllus campestris L. (Orthoptera, Gryllidae). II. Acoustic orientation of female crickets after occlusion of single sound entrances. J Comp Physiol 152:257–264

    Google Scholar 

  • Shuvalov VF, Popov VA (1971) Reaction of females of the domestic cricketAcheta domesticus to sound signals and its changes in ontogenesis. Zh Evol Biokhimi Fiziol 7:612–616

    Google Scholar 

  • Silver SC, Kühne R, Lewis DB (1984) Two-tone interactions and song coding in identified ventral cord neurones in the cricket. Acoustic Letters 7:135–140

    Google Scholar 

  • Stout JF, DeHaan CH, McGhee RW (1983) Attractiveness of the maleAcheta domesticus calling song to females. I. Dependence on each of the calling song features. J Comp Physiol 153:509–521

    Google Scholar 

  • Stout JF, Atkins G, Burghardt F (1985) The characterization and possible importance for phonotaxis of ‘L’-shaped ascending acoustic interneurons in the cricketAcheta domesticus. In: Kalmring K, Elsner N (eds) Acoustic and vibrational communication in insects. Parey, Berlin Hamburg, pp 89–100

    Google Scholar 

  • Taylor R (1968) Water vibration: a neurophysiological study of unrestrained crayfish. Comp Biochem Physiol 27:795–805

    Google Scholar 

  • Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378

    Google Scholar 

  • Tomioka K, Yamaguchi T (1984) Response modification of cricket sensory interneurons during flight. Zool Sci 1:169–186

    Google Scholar 

  • Ulagaraj SM, Walker TJ (1973) Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182:1278–1279

    Google Scholar 

  • Wiese K (1981) Influence of vibration on cricket hearing: interaction of low frequency vibration and acoustic stimuli in the omega neuron. J Comp Physiol 143:135–142

    Google Scholar 

  • Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket,Gryllus campestris L. J Comp Physiol 146:161–173

    Google Scholar 

  • Wohlers DW, Huber F (1985) Topographical organization of the auditory pathway within the prothoracic ganglion of the cricketGryllus campestris L. Cell Tissue Res 239:555–565

    Google Scholar 

  • Wolf H, Helverson O von (1986) ‘Switching-off’ of an auditory interneuron during stridulation in the acridid grasshopperChorthippus biguttulus L. J Comp Physiol A 158:861–871

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Atkins, G., Pollack, G.S. Response properties of prothoracic, interganglionic, sound-activated interneurons in the cricketTeleogryllus oceanicus . J. Comp. Physiol. 161, 681–693 (1987). https://doi.org/10.1007/BF00605009

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00605009

Keywords

Navigation