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The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria

I. Anatomy of the system

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Summary

  1. 1.

    The cerci of locusts are paired, unsegmented, cone-shaped structures arising from a depression on either side of the tip of the abdomen (Fig. 2).

  2. 2.

    The cerci bear hair sensilla of two basic types (Fig. 3): (a) filiform hairs, which emerge from a cuticular pit, are flexibly mounted, and are sensitive to wind and to mechanical displacement; and (b) bristle (or trichoid) hairs, which originate directly from the surface of the cercus, and are less flexibly mounted. The axons of neurones innervating these hairs group together into successively larger bundles before joining the cercal nerve which runs to the terminal ganglion (Fig. 4).

  3. 3.

    In the terminal ganglion the majority of cercal afferents (Fig. 5), and all identified filiform afferents (Fig. 6) end in contact with a cercal glomerulus formed by the densely interwoven arborizations of giant and non-giant interneurones (Figs. 5, 7,9).

  4. 4.

    A transverse section of the ventral nerve cord anterior to the terminal ganglion reveals four axons, one medial and three grouped together dorsolaterally, with distinctly larger profiles than all the others (Figs. 8, 9). The somata associated with these axons are located contralaterally in the terminal ganglion. All four interneurones have at least some projections into both cercal glomeruli. The soma of giant interneurone 1 (GIN 1), which is associated with the large medial axon, lies laterally in neuromere 9, the somata of GINs 2–4 are located ventrally in neuromere 9, ventrally in neuromere 10, and postero-dorsally in neuromere 11, respectively (Figs. 7,9).

  5. 5.

    All four GINs run the length of the ventral nerve cord (Figs. 10, 11, 12) and end in the brain (Fig. 11). The axon of GIN 1 is found in the ventral intermediate tract (VIT), those of GINs 2, 3, 4 are initially in the lateral dorsal tract (LDT) but they cross to the dorsal intermediate tract (DIT) at the level of the most anterior free abdominal ganglion. All have medial branches in the abdominal ganglia (Figs. 10, 12). GIN 1 has a lateral branch (sometimes absent) only in the metathoracic ganglion, while the other GINs have lateral branches in all of the thoracic ganglia (Figs. 10, 11, 12).

  6. 6.

    The cercal receptor/giant interneurone system ofLocusta is compared to those of other orthopteroid insects, with special attention to the origin and evolution of giant interneurones.

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References

  • Altman J (1983) Sensory inputs and the generation of the locust flight motor pattern: from the past to the future. In: Nachtigall W (ed) Biona Report 2. Gustav Fischer, Stuttgart, pp 127–136

    Google Scholar 

  • Altman JS, Tyrer NM (1980) Filling selected neurons with cobalt through cut axons. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques: insect nervous system. Springer, New York Heidelberg Berlin, pp 373–402

    Google Scholar 

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

    Google Scholar 

  • Bacon JP, Murphey RK (1984) Receptive fields of cricket (Acheta domesticus) interneurones are related to their dendritic structure. J Physiol 352:601–623

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Blagburn JM, Sattelle DB (1987) Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach,Periplaneta americana. J Exp Biol 127:135–157

    Google Scholar 

  • Blagburn JM, Beadle DJ, Sattelle DB (1986) Differential synaptic input of filiform hair sensory neurones onto giant interneurones in the first-instar cockroach. J Insect Physiol 32:591–595

    Google Scholar 

  • Boeckh J, Ernst K-D (1987) Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A 161:549–565

    Google Scholar 

  • Boyan GS (1983) Postembryonic development in the auditory system of the locust. J Comp Physiol 151:499–513

    Google Scholar 

  • Boyan GS (1988) Presynaptic inhibition of identified wind-sensitive afferents in the cercal system of the locust. J Neurosci 8:2748–2757

    Google Scholar 

  • Boyan GS, Ball EE (1986) Wind-sensitive interneurones in the terminal ganglion of praying mantids. J Comp Physiol A 159:773–789

    Google Scholar 

  • Boyan GS, Ball EE (1989a) Parallel inputs shape the response of a giant interneurone in the cercal system of the locust. J Insect Physiol 35:305–312

    Google Scholar 

  • Boyan GS, Ball EE (1989b) The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria. II. Physiology of giant interneurones. J Comp Physiol A 165:511–521

    Google Scholar 

  • Boyan GS, Ball EE (1989c) The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria. III. Cercal activation of thoracic motor pathways. J Comp Physiol A 165:523–537

    Google Scholar 

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

    Google Scholar 

  • Boyan GS, Williams JLD, Ball EE (1989) The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria. IV. The non-giant interneurones. J Comp Physiol A 165:539–552

    Google Scholar 

  • Callec J (1974) Synaptic transmission in the central nervous system of insects. In: Treherne JE (ed) Insect neurobiology. North-Holland, Amsterdam, pp 119–185

    Google Scholar 

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

    Google Scholar 

  • Camhi JM (1984) Neuroethology: nerve cells and the natural behavior of animals. Sinauer, Sunderland

    Google Scholar 

  • Collin SP (1985) The central morphology of the giant interneurons and their spatial relationship with the thoracic motorneurons in the cockroach,Periplaneta americana (Insecta). J Neurobiol 16:249–267

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Doe CQ, Goodman CS (1985) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205

    Google Scholar 

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

    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 

  • Edwards JS, Williams L (1981) Anterior-most projections of giant interneurones inAcheta domesticus terminate in mechano-receptor neuropile of the brain. Soc Neurosci Abstr 7:252

    Google Scholar 

  • Fuller H, Ernst A (1977) Die Ultrastruktur der cercalen Cuticularsensillen vonPeriplaneta americana (L.). Zool Jb Anat 98:544–571

    Google Scholar 

  • Gnatzy W (1976) The ultrastructure of the thread-hairs on the cerci of the cockroachPeriplaneta americana L.: the intermoult phase. J Ultrastruct Res 54:124–134

    Google Scholar 

  • Gnatzy W, Schmidt K (1971) Die Feinstruktur der Sinneshaare auf den Cerci vonGryllus bimaculatus Degx. (Saltatoria, Gryllidae). I. Faden- und Keulenhaare. Z Zellforsch 122:190–209

    Google Scholar 

  • Hartman HB, Bennett LP, Moulton BA (1987) Anatomy of equilibrium receptors and cerci of the burrowing desert cockroachArenavaga (Insecta, Blattodea). Zoomorphology 107:81–87

    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 

  • Heusslein R, Gnatzy W (1987) Central projections of campaniform sensilla on the cerci of crickets and cockroaches. Cell Tissue Res 247:591–598

    Google Scholar 

  • Hoyle G (1958) The leap of the grasshopper. Sci Am 198:30–35

    Google Scholar 

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

  • Jacobs GA, Miller JP (1985) Functional properties of individual neuronal branches isolated in situ by laser photoinactivation. Science 228:344–346

    Google Scholar 

  • Jacobs GA, Murphey RK (1987) Segmental origins of the cricket giant interneuron system. J Comp Neurol 265:145–157

    Google Scholar 

  • Jacobs GA, Miller JP, Murphey RK (1986) Integrative mechanisms controlling directional sensitivity of an identified sensory interneuron. J Neurosci 6:2298–2311

    Google Scholar 

  • Kirk MD (1985) Presynaptic inhibition in the crayfish CNS: pathways and synaptic mechanisms. J Neurophysiol 54:1305–1325

    Google Scholar 

  • Krenz WD, Reichert H (1985) Lateralized inhibitory input to an identified nonspiking local interneuron in the crayfish mechanosensory system. J Comp Physiol A 157:499–508

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Murphey RK (1981) The structure and development of a somatotopic map in crickets: the cercal afferent projection. Dev Biol 88:236–246

    Google Scholar 

  • Murphey RK (1985) A second cricket cercal sensory system: bristle hairs and the interneurons they activate. J Comp Physiol A 156:357–367

    Google Scholar 

  • O'Shea M, Williams JLD (1974) The anatomy and output connection of a locust visual interneurone; the Lobula Giant Movement Detector (LGMD) neurone. J Comp Physiol 91:257–266

    Google Scholar 

  • O'Shea M, Rowell CHF, Williams JLD (1974) The anatomy of a locust visual interneurone; the descending contralateral movement detector. J Exp Biol 60:1–12

    Google Scholar 

  • Palka J, Levine R, Schubiger M (1977) The cercus-to-giant interneuron system of crickets. J Comp Physiol 119:267–283

    Google Scholar 

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

    Google Scholar 

  • Reichert H, Plummer MR, Hagiwara G, Roth RL, Wine JJ (1982) Local interneurons in the terminal abdominal ganglion of the crayfish. J Comp Physiol 149:145–162

    Google Scholar 

  • Reichert H, Plummer MR, Wine JJ (1983) Identified nonspiking local interneurons mediate nonrecurrent, lateral inhibition of crayfish mechanosensory interneurons. J Comp Physiol 151:261–276

    Google Scholar 

  • Ritzmann RE (1984) The cockroach escape response. In: Eaton RC (ed) Neural mechanisms of startle behavior. Plenum, New York London, pp 93–131

    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, 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 

  • Roonwal ML (1937) Studies on the embryology of the African migratory locust,Locusta migratoria migratorioides Reiche and Frm. (Orthoptera, Acrididae). II. Organogeny. Phil Trans R Soc Lond B 227:157–244

    Google Scholar 

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

    Google Scholar 

  • Sakaguchi DS, Murphey RK (1983) The equilibrium detecting system of the cricket. Physiology and morphology of an identified interneuron. J Comp Physiol 150:141–152

    Google Scholar 

  • Schmidt K, Gnatzy W (1972) Die Feinstruktur der Sinneshaare auf den Cerci vonGryllus bimaculatus Deg. (Saltatoria, Gryllidae). III. Die kurzen Borstenhaare. Z Zellforsch 126:206–222

    Google Scholar 

  • Seabrook WD (1968) The innervation of the terminal abdominal segments (VIII–XI) of the desert locust,Schistocerca gregaria. Can Entomol 100:693–715

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Shankland M (1981) Development of a sensory afferent projection in the grasshopper embryo. II. Growth and branching of peripheral sensory axons within the central nervous system. J Embryol Exp Morphol 64:187–209

    Google Scholar 

  • Shankland M, Bentley D (1983) Sensory receptor differentiation and axonal pathfinding in the cercus of the grasshopper embryo. Dev Biol 97:468–482

    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 

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

    Google Scholar 

  • Shepherd D, Kämper G, Murphey RK (1988) The synaptic origins of receptive field properties in the cricket cercal sensory system. J Comp Physiol A 162:1–11

    Google Scholar 

  • Shimozawa T, Kanou M (1984a) Varieties of filiform hairs: range fractionation by sensory afferents and cercal interneurons of a cricket. J Comp Physiol A 155:485–493

    Google Scholar 

  • Shimozawa T, Kanou M (1984b) The aerodynamics and sensory physiology of range fractionation in the cercal filiform sensilla of the cricketGryllus bimaculatus. J Comp Physiol A 155:495–505

    Google Scholar 

  • Sihler H (1924) Die Sinnesorgane an den Cerci der Insekten. Zool Jb Anat 45:519–580

    Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Thomas JG (1965) The abdomen of the female desert locust (Schistocerca gregaria Forskål) with special reference to the sense organs. Anti-Locust Bull 42:1–20

    Google Scholar 

  • Tyrer NM, Bell EM (1974) The intensification of profiles of cobalt-filled neurons in sectioned material. Brain Res 73:151–155

    Google Scholar 

  • Tyrer NM, Gregory GE (1982) A guide to the neuroanatomy of locust subesophageal and thoracic ganglia. Phil Trans R Soc Lond B 297:91–124

    Google Scholar 

  • Watson AHD, Pflüger H-J (1987) The distribution of GABA-like immunoreactivity in relation to ganglion structure in the abdominal nerve cord of the locust (Schistocerca gregaria). Cell Tissue Res 249:391–402

    Google Scholar 

  • Westin J (1979) Responses to wind recorded from the cercal nerve of the cockroachPeriplaneta americana. I. Response properties of single sensory neurons. J Comp Physiol 133:97–102

    Google Scholar 

  • Wine JJ (1984) The structural basis of an innate behavioural pattern. J Exp Biol 112:283–319

    Google Scholar 

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Boyan, G.S., Williams, J.L.D. & Ball, E.E. The wind-sensitive cercal receptor/giant interneurone system of the locust,Locusta migratoria . J. Comp. Physiol. 165, 495–510 (1989). https://doi.org/10.1007/BF00611237

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