Summary
-
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.
Transverse sections of connectives reveal nine large axon profiles whose spatial relationship changes along the ventral nerve cord (Fig. 4).
-
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.
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.
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.
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.
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.
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.
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).
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurons in wholemount preparations. Brain Res 138:359–363
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
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
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
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
Blackith RE, Blackith RM (1968) A numerical taxonomy of orthopteroid insects. Aust J Zool 16:111–131
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
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
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
Camhi JM (1980) The escape system of the cockroach. Sci Am 243:144–157
Camhi JM, Nolen TG (1981) Properties of the escape system of cockroaches during walking. J Comp Physiol 142:339–346
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
Comer CM (1985) Analyzing cockroach escape behavior with lesions of individual giant interneurons. Brain Res 335:342–346
Cook PM (1951) Observations on giant fibres of the nervous system ofLocusta migratoria. Q J Microsc Soc 92:297–305
Counter SA (1976) An electrophysiological study of sound sensitive neurons in the ‘primitive ear’ ofAcheta domesticus. J Insect Physiol 22:1–18
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
Dagan D, Parnas I (1974) After effects of spikes in cockroach giant axons. J Neurobiol 5:95–105
Daley DL (1982) Neural basis of wind-receptive fields of cockroach giant interneurons. Brain Res 238:211–216
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
Edwards JS, Ball E (1980) Cercal sensory projections in Dermaptera and Notoptera. Soc Neurosci Abstr 6:220
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
Edwards JS, Palka J (1971) Neural regeneration: delayed formation of central contacts by insect sensory cells. Science 172:591–594
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
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
Farley RD, Case JF (1968) Sensory modulation of ventilative pacemaker output in the cockroach,Periplaneta americana. J Insect Physiol 14:591–601
Farley RD, Milburn NS (1969) Structure and function of the giant fibre system in the cockroach,Periplaneta americana. J Insect Physiol 15:457–476
Fielden A (1960) Transmission through the last abdominal ganglion of the dragonfly nymph,Anax imperator. J Exp Biol 37:832–844
Fitch GK, Kammer AE (1982) Modulation of the ventilatory rhythm of the hellgrammiteCorydalus cornutus by mechanosensory input. J Comp Physiol 149:423–434
Fraser P (1977) Cereal ablation modifies tethered flight behaviour of cockroach. Nature 268:523–524
Grillner S, Wallén P (1984) How does the lamprey central nervous system make the lamprey swim? J Exp Biol 112:337–357
Guthrie DM (1966) Sound production and reception in a cockroach. J Exp Biol 45:321–328
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
Horridge GA, Burrows M (1974) Synapses upon motoneurons of locusts during retrograde degeneration. Philos Trans R Soc Lond B 269:95–108
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
Jacobs G, Murphey RK (1981) Development of the giant fiber system in crickets. Soc Neurosci Abstr 7:4
Jacobs GA, Redfern C, Miller JP (1985) Identification and characterization of inhibitory inputs in the cricket cercal afferent system. Soc Neurosci Abstr 11:164
Kamp JW (1973) Numerical classification of the orthopteroids with special reference to the Grylloblattodea. Can Entomol 105:1235–1249
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
Katayama Y (1971) Recovery course of excitability in a single neurone ofOnchidium verruculatum. J Exp Biol 54:471–484
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
Kristensen NP (1981) Phylogeny of insect orders. Annu Rev Entomol 26:135–158
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
Levine RB, Murphey RK (1980) Pre- and postsynaptic inhibition of identified giant interneurons in the cricket (Achetadomesticus). J Comp Physiol 135:269–282
Matsumoto SG, Murphey RK (1977) Sensory deprivation during development decreases the responsiveness of cricket giant interneurones. J Physiol 268:533–548
Matsumoto SG, Murphey RK (1978) Sensory deprivation in the cricket nervous system: evidence for a critical period. J Physiol 285:159–170
McCrohan CR (1984) Initiation of feeding motor output by an identified interneurone in the snailLymnaea stagnalis. J Exp Biol 113:351–366
Mendenhall B, Murphey RK (1974) The morphology of cricket giant interneurons. J Neurobiology 5:565–580
Miller JP, Jacobs GA (1984) Relationships between neuronal structure and function. J Exp Biol 112:129–145
Murphey RK (1985) Competition and chemoaffinity in insect sensory systems. Trends in Neurosci 8:120–125
Murphey RK, Matsumoto SG (1976) Experience modifies the plastic properties of identified neurons. Science 191:564–566
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
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
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
Murphey RK, Bacon JP, Johnson SE (1985) Ectopic neurons and the organization of insect sensory systems. J Comp Physiol A 156:381–389
Narahashi T (1960) Excitation and electrical properties of giant axon of cockroaches. In: Electrical activity of single cells. Igakushoin, Hongo, Tokyo, pp 119–131
Nesbitt HHJ (1941) A comparative morphological study of the nervous system of the Orthoptera and related orders. Ann Entomol Soc Am 34:51–81
Nocke H (1975) Physical and physiological properties of the tettigoniid (‘Grasshopper’) ear. J Comp Physiol 100:25–57
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
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
Pearson KG, Stein RB, Malhotra SK (1970) Properties of action potentials from insect motor nerve fibres. J Exp Biol 53:299–316
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
Pinsker HM, Ayers J (1983) Neuronal oscillators. In: Willis WD (ed) The clinical neurosciences. Neurobiology. Churchill Livingstone, New York, pp 203–266
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
Ritzmann RE, Camhi JM (1978) Excitation of leg motor neurons by giant interneurons in the cockroachPeriplaneta americana. J Comp Physiol 125:305–316
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
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
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
Roeder KD (1948) Organization of the ascending giant fiber system in the cockroach,Periplaneta americana. J Exp Zool 108:243–262
Roeder KD, Tozian L, Weiant EA (1960) Endogenous nerve activity and behaviour in the mantis and cockroach. J Insect Physiol 4:45–62
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
Schwab WE, Josephson RK (1977) Coding of acoustic information in cockroach giant fibres. J Insect Physiol 23:665–670
Seabrook WD (1970) The structure of the terminal ganglionic mass of the locust,Schistocerca gregaria (Forskal). J Comp Neurol 138:63–86
Seabrook WD (1971) An electrophysiological study of the giant fiber system of the locustSchistocerca gregaria. Can I Zool 49:555–560
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
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
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
Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759
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
Tobias ML, Ritzmann RE (1984) Responses of mesothoracic motor neurons to giant interneuron stimulation in the cockroach. J Comp Physiol A 154:633–640
Viallanes H (1891) Sur quelques points de l'histoire du développement embryonnaire de la Mante religieuse. Ann Sci Nat Zool 2:283–328
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
Wilson DM (1962) Bifunctional muscles in the thorax of grasshoppers. J Exp Biol 39:669–677
Wilson JA (1979) The structure and function of serially homologous leg motor neurons in the locust. I. Anatomy. J Neurobiol 10:41–65
Wilson JA, Hoyle G (1978) Serially homologous neurones as concomitants of functional specialisation. Nature 274:377–379
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00603731