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Wind-sensitive interneurones in the terminal ganglion of praying mantids

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Summary

  1. 1.

    Twelve types of wind-sensitive neurone have been identified in the terminal ganglion of the mantids,Archimantis sobrina andA. latistylus (Fig. 1). Nine have conspicuously larger axons than the others in the connective of the ventral nerve cord and are termed ‘giant’ interneurones (Figs. 1, 2, 3), although they are small by comparison with those of other orthopteroid insects (Fig. 15).

  2. 2.

    Transverse sections of connectives reveal nine large axon profiles whose spatial relationship changes along the ventral nerve cord (Fig. 4).

  3. 3.

    Transverse sections of ganglia containing stained giant cells show that major arborizations are found in neuropilar regions containing the terminals of cereal afferents (Fig. 5).

  4. 4.

    Recorded cells could be divided into two groups depending on whether their responses to wind stimuli were purely excitatory (Figs. 6, 7), or contained an inhibitory component (El responses, Fig. 8). Electrical stimulation of cercal afferents confirmed the response patterns evoked by wind (Figs. 7, 8 and 9).

  5. 5.

    Dendritic arborizations are more strongly developed on the side of major synaptic input to each giant cell (Figs. 1, 2, 5) as established by electrical and wind stimulation of afferents in left and right cerci (Fig. 10).

  6. 6.

    Conduction velocities in the giant cells ranged from 2.5–3.1 m/s (Fig. 11, Table 1).These neurones are thus amongst the slowest conducting insect giant neurones, consistent with their small diameter relative to those of other insects (Fig. 15).

  7. 7.

    The short response latencies and the 1∶1 nature of their response to high frequency (100 Hz) electrical stimulation of the cereal nerve indicated that at least neurone Types 5, 8 and 11 (Fig. 11, Table 1) probably have direct connections with cereal receptors.

  8. 8.

    Several cells had high rates of spontaneous activity and in one (Type 5, Fig. 12A), injection of hyperpolarizing current produced a rhythmical bursting at approximately half the spontaneous rate. The interburst interval could be altered by phasic stimulation of the cereal nerve (Fig. 12 B).

  9. 9.

    Behavioural experiments with a tethered mantid showed responses in leg- and flight-motor pathways to wind stimulation of the cerci. In a dissected preparation, electrical stimulation of abdominal connectives and wind stimulation of the cerci both evoked responses in four neurones of the metathoracic ganglion: one spiking local interneurone and three motoneurones (Figs. 13, 14).

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References

  • Andersson O, Forssberg H, Grillner S, Wallén P (1981) Peripheral feedback mechanisms acting on the central pattern generator for locomotion in fish and cat. Can J Physiol Pharmacol 59:713–726

    Google Scholar 

  • Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurons in wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Ball EE, Stone RC (1982) The cereal receptor system of the praying mantid,Archimantis brunneriana Sauss. I. Cereal morphology and receptor types. Cell Tissue Res 224:55–70

    Google Scholar 

  • Ball EE, Boyan GS, Stone RC (1982) The cereal receptor system of the praying mantid,Archimantis brunneriana Sauss. II. Cereal nerve structure and projection and electrophysiological responses of individual receptors. Cell Tissue Res 224:71–80

    Google Scholar 

  • Belosky DC, Delcomyn F (1977) Information processing in a cricket ganglion: the responses of giant fibres to sound pulses. J Insect Physiol 23:359–365

    Google Scholar 

  • Bernard J, Gobin B, Callec JJ (1983) A chordotonal organ inhibits giant interneurones in the sixth abdominal ganglion of the cockroach. J Comp Physiol 153:377–383

    Google Scholar 

  • Blackith RE, Blackith RM (1968) A numerical taxonomy of orthopteroid insects. Aust J Zool 16:111–131

    Google Scholar 

  • Boyan GS, Ashman S, Ball EE (1986) Initiation and modulation of flight by a single giant interneuron in the cereal system of the locust. Naturwissenschaften 73:272–274

    Google Scholar 

  • Callec JJ (1985) Synaptic transmission in the central nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Chap 5, vol 5, Nervous system: structure and function, Pergamon, Oxford, pp 139–179

    Google Scholar 

  • Callec JJ, Boistel J (1966) Phénomènes d'excitation et d'inhibition au niveau du dernier ganglion abdominal de la blatte,Periplaneta americana L. C R Soc Biol 160:2418–2424

    Google Scholar 

  • Camhi JM (1980) The escape system of the cockroach. Sci Am 243:144–157

    Google Scholar 

  • Camhi JM, Nolen TG (1981) Properties of the escape system of cockroaches during walking. J Comp Physiol 142:339–346

    Google Scholar 

  • Cloarec A (1968) Étude structurale de la dernière masse ganglionaire de la chaine nerveuse abdominale deMantis religiosa L. Bull Soc Zool France 93:331–346

    Google Scholar 

  • Comer CM (1985) Analyzing cockroach escape behavior with lesions of individual giant interneurons. Brain Res 335:342–346

    Google Scholar 

  • Cook PM (1951) Observations on giant fibres of the nervous system ofLocusta migratoria. Q J Microsc Soc 92:297–305

    Google Scholar 

  • Counter SA (1976) An electrophysiological study of sound sensitive neurons in the ‘primitive ear’ ofAcheta domesticus. J Insect Physiol 22:1–18

    Google Scholar 

  • Dagan D, Parnas I (1970) Giant fibre and small fibre pathways involved in the evasive response of the cockroach,Periplaneta americana. J Exp Biol 52:313–324

    Google Scholar 

  • Dagan D, Parnas I (1974) After effects of spikes in cockroach giant axons. J Neurobiol 5:95–105

    Google Scholar 

  • Daley DL (1982) Neural basis of wind-receptive fields of cockroach giant interneurons. Brain Res 238:211–216

    Google Scholar 

  • Daley DL, Vardi N, Appignani B, Camhi JM (1981) Morphology of the giant interneurons and cereal nerve projections of the American cockroach. J Comp Neurol 196:41–52

    Google Scholar 

  • Edwards JS, Ball E (1980) Cercal sensory projections in Dermaptera and Notoptera. Soc Neurosci Abstr 6:220

    Google Scholar 

  • Edwards JS, Mann D (1981) The structure of the cereal sensory system and ventral nerve cord ofGrylloblatta. A comparative study. Cell Tissue Res 217:177–188

    Google Scholar 

  • Edwards JS, Palka J (1971) Neural regeneration: delayed formation of central contacts by insect sensory cells. Science 172:591–594

    Google Scholar 

  • Edwards JS, Palka J (1974) The cerci and abdominal giant fibres of the house cricketAcheta domesticus. I. Anatomy and physiology of normal adults. Proc R Soc Lond B 185:83–103

    Google Scholar 

  • Edwards JS, Reddy GJ (1986) Mechanosensory appendages and giant interneurons in the firebrat (Thermobia domestica, Thysanura): a prototype system for terrestrial predator evasion. J Comp Neurol 243:535–546

    Google Scholar 

  • Farley RD, Case JF (1968) Sensory modulation of ventilative pacemaker output in the cockroach,Periplaneta americana. J Insect Physiol 14:591–601

    Google Scholar 

  • Farley RD, Milburn NS (1969) Structure and function of the giant fibre system in the cockroach,Periplaneta americana. J Insect Physiol 15:457–476

    Google Scholar 

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

    Google Scholar 

  • Fitch GK, Kammer AE (1982) Modulation of the ventilatory rhythm of the hellgrammiteCorydalus cornutus by mechanosensory input. J Comp Physiol 149:423–434

    Google Scholar 

  • Fraser P (1977) Cereal ablation modifies tethered flight behaviour of cockroach. Nature 268:523–524

    Google Scholar 

  • Grillner S, Wallén P (1984) How does the lamprey central nervous system make the lamprey swim? J Exp Biol 112:337–357

    Google Scholar 

  • Guthrie DM (1966) Sound production and reception in a cockroach. J Exp Biol 45:321–328

    Google Scholar 

  • Harrow ID, Sattelle DB (1983) Acetylcholine receptors on the cell body membrane of giant interneurone 2 in the cockroach,Periplaneta americana. J Exp Biol 105:339–350

    Google Scholar 

  • Horridge GA, Burrows M (1974) Synapses upon motoneurons of locusts during retrograde degeneration. Philos Trans R Soc Lond B 269:95–108

    Google Scholar 

  • Hue B (1983) Electrophysiologie et pharmacologie de la transmission synaptique dans le système nerveux central de la blatte,Periplaneta americana L. Doctoral Thesis, University of Angers

  • Iles JF (1972) Structure and synaptic activation of the fast coxal depressor motoneurone of the cockroach,Periplaneta americana. J Exp Biol 56:647–656

    Google Scholar 

  • Jacobs G, Murphey RK (1981) Development of the giant fiber system in crickets. Soc Neurosci Abstr 7:4

    Google Scholar 

  • Jacobs GA, Redfern C, Miller JP (1985) Identification and characterization of inhibitory inputs in the cricket cercal afferent system. Soc Neurosci Abstr 11:164

    Google Scholar 

  • Kamp JW (1973) Numerical classification of the orthopteroids with special reference to the Grylloblattodea. Can Entomol 105:1235–1249

    Google Scholar 

  • Kämper G (1984) Abdominal ascending interneurons in crickets: responses to sound at the 30-Hz calling song frequency. J Comp Physiol A 155:507–520

    Google Scholar 

  • Katayama Y (1971) Recovery course of excitability in a single neurone ofOnchidium verruculatum. J Exp Biol 54:471–484

    Google Scholar 

  • Kevan DK McE (1977) The higher classification of the orthopteroid insects: a general view. In: Kevan DK McE (ed) The higher classification of the orthopteroid insects. Lyman Entomological Museum and Research Laboratory Memoir No. 4, McGill Univ Quebec

  • Kristensen NP (1975) The phylogeny of hexapod “orders”. A critical review of recent accounts. Z Zool Syst Evolut-forsch 13:1–43

    Google Scholar 

  • Kristensen NP (1981) Phylogeny of insect orders. Annu Rev Entomol 26:135–158

    Google Scholar 

  • Kukalová-Peck J (1985) Ephemeroid wing venation based upon new gigantic Carboniferous mayflies and basic morphology, phylogeny, and metamorphosis of pterygote insects (Insecta, Ephemerida). Can J Zool 63:933–955

    Google Scholar 

  • Levine RB, Murphey RK (1980) Pre- and postsynaptic inhibition of identified giant interneurons in the cricket (Achetadomesticus). J Comp Physiol 135:269–282

    Google Scholar 

  • Matsumoto SG, Murphey RK (1977) Sensory deprivation during development decreases the responsiveness of cricket giant interneurones. J Physiol 268:533–548

    Google Scholar 

  • Matsumoto SG, Murphey RK (1978) Sensory deprivation in the cricket nervous system: evidence for a critical period. J Physiol 285:159–170

    Google Scholar 

  • McCrohan CR (1984) Initiation of feeding motor output by an identified interneurone in the snailLymnaea stagnalis. J Exp Biol 113:351–366

    Google Scholar 

  • Mendenhall B, Murphey RK (1974) The morphology of cricket giant interneurons. J Neurobiology 5:565–580

    Google Scholar 

  • Miller JP, Jacobs GA (1984) Relationships between neuronal structure and function. J Exp Biol 112:129–145

    Google Scholar 

  • Murphey RK (1985) Competition and chemoaffinity in insect sensory systems. Trends in Neurosci 8:120–125

    Google Scholar 

  • Murphey RK, Matsumoto SG (1976) Experience modifies the plastic properties of identified neurons. Science 191:564–566

    Google Scholar 

  • Murphey RK, Matsumoto SG, Mendenhall B (1976) Recovery from deafferentation by cricket interneurons after reinnervation by their peripheral field. J Comp Neurol 169:335–346

    Google Scholar 

  • Murphey RK, Palka J, Hustert R (1977) The cercus-to-giant interneuron system of crickets. II. Response characteristics of two giant interneurons. J Comp Physiol 119:285–300

    Google Scholar 

  • Murphey RK, Johnson SE, Walthall WW (1981) The effects of transplantation and regeneration of sensory neurons on a somatotopic map in the cricket central nervous system. Dev Biol 88:247–258

    Google Scholar 

  • Murphey RK, Bacon JP, Johnson SE (1985) Ectopic neurons and the organization of insect sensory systems. J Comp Physiol A 156:381–389

    Google Scholar 

  • Narahashi T (1960) Excitation and electrical properties of giant axon of cockroaches. In: Electrical activity of single cells. Igakushoin, Hongo, Tokyo, pp 119–131

    Google Scholar 

  • Nesbitt HHJ (1941) A comparative morphological study of the nervous system of the Orthoptera and related orders. Ann Entomol Soc Am 34:51–81

    Google Scholar 

  • Nocke H (1975) Physical and physiological properties of the tettigoniid (‘Grasshopper’) ear. J Comp Physiol 100:25–57

    Google Scholar 

  • Palka J, Edwards JS (1974) The cerci and abdominal giant fibres of the house cricket,Acheta domesticus. II. Regeneration and effects of chronic deprivation. Proc R Soc Lond B 185:105–121

    Google Scholar 

  • Pearson KG, Reye DN, Robertson RM (1983) Phase-dependent influences of wing stretch receptors on flight rhythm in the locust. J Neurophysiol 49:1168–1181

    Google Scholar 

  • Pearson KG, Stein RB, Malhotra SK (1970) Properties of action potentials from insect motor nerve fibres. J Exp Biol 53:299–316

    Google Scholar 

  • 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 233:133–145

    Google Scholar 

  • Pinsker HM, Ayers J (1983) Neuronal oscillators. In: Willis WD (ed) The clinical neurosciences. Neurobiology. Churchill Livingstone, New York, pp 203–266

    Google Scholar 

  • Potente A (1975) Untersuchungen zur Morphologie der cercalen Riesenfasern im Bauchmark vonLocusta migratoria. Hausarbeit, Ruhr-Universität Bochum

  • Ritzmann RE (1981) Motor responses to paired stimulation of giant interneurons in the cockroachPeriplaneta americana. II. The ventral giant interneurons. J Comp Physiol 143:71–80

    Google Scholar 

  • Ritzmann RE, Camhi JM (1978) Excitation of leg motor neurons by giant interneurons in the cockroachPeriplaneta americana. J Comp Physiol 125:305–316

    Google Scholar 

  • Ritzmann RE, Pollack AJ (1981) Motor responses to paired stimulation of giant interneurons in the cockroachPeriplaneta americana. I. The dorsal giant interneurons. J Comp Physiol 143:61–70

    Google Scholar 

  • Ritzmann RE, Tobias ML, Fourtner CR (1980) Flight activity initiated via giant interneurons of the cockroach: evidence for bifunctional trigger interneurons. Science 210:443–445

    Google Scholar 

  • Ritzmann RE, Pollack AJ, Tobias ML (1982) Flight activity mediated by intracellular stimulation of dorsal giant interneurons of the cockroachPeriplaneta americana. J Comp Physiol 147:313–322

    Google Scholar 

  • Roeder KD (1948) Organization of the ascending giant fiber system in the cockroach,Periplaneta americana. J Exp Zool 108:243–262

    Google Scholar 

  • Roeder KD, Tozian L, Weiant EA (1960) Endogenous nerve activity and behaviour in the mantis and cockroach. J Insect Physiol 4:45–62

    Google Scholar 

  • Rozhkova GI, Rodionova HI, Popov AV (1984) Two types of information processing in cereal systems of insects: directional sensitivity of giant interneurons. J Comp Physiol A 154:805–815

    Google Scholar 

  • Schwab WE, Josephson RK (1977) Coding of acoustic information in cockroach giant fibres. J Insect Physiol 23:665–670

    Google Scholar 

  • Seabrook WD (1970) The structure of the terminal ganglionic mass of the locust,Schistocerca gregaria (Forskal). J Comp Neurol 138:63–86

    Google Scholar 

  • Seabrook WD (1971) An electrophysiological study of the giant fiber system of the locustSchistocerca gregaria. Can I Zool 49:555–560

    Google Scholar 

  • Shankland M, Goodman CS (1982) Development of the dendritic branching pattern of the medial giant interneuron in the grasshopper embryo. Dev Biol 92:489–506

    Google Scholar 

  • Shankland M, Bentley D, Goodman CS (1982) Afferent innervation shapes the dendritic branching pattern of the medial giant interneuron in grasshopper embryos raised in culture. Dev Biol 92:507–520

    Google Scholar 

  • Sharov AG (1971) Phylogeny of the Orthopteroidea. Rodendorf BB (ed). Jerusalem, Israel Program for Scientific Translations

  • Shen J-X (1983) The cercus-to-giant interneuron system in the bushcricketTettigonia cantans: morphology and response to low-frequency sound. J Comp Physiol 151:449–459

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Tobias M, Murphey RK (1979) The response of cercal receptors and identified interneurons in the cricket (Acheta domesticus) to airstreams. J Comp Physiol 129:51–59

    Google Scholar 

  • Tobias ML, Ritzmann RE (1984) Responses of mesothoracic motor neurons to giant interneuron stimulation in the cockroach. J Comp Physiol A 154:633–640

    Google Scholar 

  • Viallanes H (1891) Sur quelques points de l'histoire du développement embryonnaire de la Mante religieuse. Ann Sci Nat Zool 2:283–328

    Google Scholar 

  • Westin J, Langberg JJ, Camhi JM (1977) Response of giant interneurons of the cockroachPeriplaneta americana to wind puffs of different directions and velocities. J Comp Physiol 121:307–324

    Google Scholar 

  • Wilson DM (1962) Bifunctional muscles in the thorax of grasshoppers. J Exp Biol 39:669–677

    Google Scholar 

  • Wilson JA (1979) The structure and function of serially homologous leg motor neurons in the locust. I. Anatomy. J Neurobiol 10:41–65

    Google Scholar 

  • Wilson JA, Hoyle G (1978) Serially homologous neurones as concomitants of functional specialisation. Nature 274:377–379

    Google Scholar 

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  1. Department of Neurobiology, Research School of Biological Sciences, Australian National University, P.O. Box 475, 2601, Canberra City, A.C.T., Australia

    G. S. Boyan & E. E. Ball

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  1. G. S. Boyan
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Boyan, G.S., Ball, E.E. Wind-sensitive interneurones in the terminal ganglion of praying mantids. J. Comp. Physiol. 159, 773–789 (1986). https://doi.org/10.1007/BF00603731

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