Mechanosensory Signal Processing: Impact on and Modulation by Pattern-Generating Networks, Exemplified in Locust Flight and Walking

Summary

In the control of locomotor movements, central pattern generating networks and sensory input interact in different ways. Sensory feedback may set the timing for the generation of central pattern elements, and in this way serve to trigger critical transitions between (centrally programmed) phases of a movement. Conversely, central network action may modulate sensory signal processing in a phase-dependent manner, and thus guarantee appropriate reflex responses at all phases of a cyclic movement. The former aspect is exemplified here by the reset of the wingbeat rhythm in the locust by input from a wing proprioceptor, the tegula. The latter aspect is illustrated by the modulatory effects a rhythmic central drive has on the processing of leg mechanosensory signals by spiking local interneurones in the locust. Both mechanisms will usually coexist and interact in the generation of the motor output, requiring close interaction of central and peripheral elements.

Certain traits of these insect motor control networks, and possibly of neural circuits in general, appear to reflect developmental and evolutionary cues, rather than genuine computational requirements. This concerns in particular the frequent observation of “weak” or “redundant” synaptic contacts in neural networks and the high degree of interconnectivity.

Keywords

Assure Pilocarpine Burrows 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arbas E.A. and Tolbert L.T. (1986). Presynaptic terminals persist following degeneration of “flight” muscle during development of a flightless grasshopper. Journal of Neurobiology 17, 627–636.PubMedCrossRefGoogle Scholar
  2. Arshavsky Y.I., Beloozerova I.N., Orlovsky G.N., Panchin Y.V. and Pavlova G.A. (1985). Control of locomotion in marine mollusc Clione limacina. III. On the origin of locomotory rhythm. Experimental Brain Research 58, 273–284.Google Scholar
  3. Bässler U. (1983). Neural basis of elementary behaviour in stick insects, ed Braitenberg V. 1–169. Springer Verlag, Berlin, Heidelberg, New York.CrossRefGoogle Scholar
  4. Bässler U. and Wegner U. (1983). Motor output of the denervated thoracic ventral nerve cord in the stick insect Carausius morosus. Journal of Experimental Biology 105, 127–145.Google Scholar
  5. Bässler U. (1993a). The femur-tibia control system of stick insects — a model system for the study of the neural basis of joint control. Brain Research Reviews 18, 207–226.PubMedCrossRefGoogle Scholar
  6. Bässler U. (1993b). The walking (and searching-) pattern generator of stick insects, a modular system composed of reflex chains and endogenous oscillators. Biological Cybernetics 69, 305–317.CrossRefGoogle Scholar
  7. Burrows M. (1989). Processing of mechanosensory signals in local reflex pathways of the locust. Journal of Experimental Biology 146, 209–227.PubMedGoogle Scholar
  8. Burrows M, and Laurent G. (1993). Synaptic potentials in the central terminals of locust proprioceptive afferents generated by other afferents from the same sense organ. Journal of Neuroscience 13, 808–819.PubMedGoogle Scholar
  9. Büschges A., Ramirez J-M., Driesang R. and Pearson K.G. (1992). Connections of the forewing tegulae in the locust flight system and their modification following partial deafferentation. Journal of Neurobiology 23, 44–60.PubMedCrossRefGoogle Scholar
  10. Clarac F., El Manira A. and Cattaert D. (1992). Presynaptic control as a mechanism of sensory-motor integration. Current Opinion in Neurobiology 2, 764–769.PubMedCrossRefGoogle Scholar
  11. Getting P.A. (1988). Comparative analysis of invertebrate central pattern generators. In: Neural control of rhythmic movements eds Cohen A.H., Rossignol S. and Grillner S. 101–127. Wiley & Sons, New York.Google Scholar
  12. Grillner S. and Rossignol S. (1978). On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Research 146, 269-277.Google Scholar
  13. Horsmann U. (1985). Der Einfluß propriozeptiver Windmessung auf den Flug der Wanderheuschrecke und die Bedeutung descendierender Neuronen der Tritocerebralcommissur. Ph.D thesis university of Cologne.Google Scholar
  14. Kutsch W., Hanloser H. and Reinecke M. (1980). Light-and electron-microscopic analysis of a complex sensory organ: the tegula of Locusta migratoria. Cell and Tissue Research 210, 461–478.PubMedCrossRefGoogle Scholar
  15. Laurent G. (1990). Voltage-dependent nonlinearities in the membrane of locust nonspiking local interneurons, and their significance for synaptic integration. Journal of Neuroscience 10, 2268–2280.PubMedGoogle Scholar
  16. Laurent G. (1993). A dendritic control mechanism in axonless neurons of the locust, Schistocerca gregaria. Journal of Physiology (Lond) 470, 45–54.Google Scholar
  17. Laurent G. and Burrows M. (1989). Intersegmental interneurons can control the gain of reflexes in adjacent segments of the locust by their action on nonspiking local interneurons. Journal of Neuroscience 9, 3030–3039.PubMedGoogle Scholar
  18. Nachtigall W. (1981). Der Vorderflügel großer Heuschrecken als Luftkrafterzeuger. I. Modellmessungen zur aerodynamischen Wirkung unterschiedlicher Flügelprofile. Journal of Comparative Physiology 142, 127–134.CrossRefGoogle Scholar
  19. Neumann L. (1985). Experiments on tegula function for flight coordination in the locust. In: Insect locomotion eds Gewecke M. and Wendler G. 149–156. Parey Verlag, Berlin, Hamburg.Google Scholar
  20. Pearson K.G. and Wolf H. (1988). Connections of hindwing tegulae with flight neurones in the locust, Locusta migratoria. Journal of Experimental Biology 135, 381–409.Google Scholar
  21. Ramirez J-M. and Pearson K.G. (1991). Octopaminergic modulation in the flight system of the locust. Journal of Neurophysiology 66, 1522–1537.PubMedGoogle Scholar
  22. Robertson R.M. and Pearson K.G. (1983). Interneurones in the flight system of the locust: distribution, connections and resetting properties. Journal of Comparative Neurology 215, 33–50.PubMedCrossRefGoogle Scholar
  23. Robertson R.M. and Pearson K.G. (1985). Neural networks controlling locomotion in locusts. In: Model neuronal networks and behaviour ed Selverston A.I. 21–35. Plenum Press, New York, London.Google Scholar
  24. Ronacher B., Wolf H. and Reichert H. (1988). Locust flight behavior after hemisection of individual thoracic ganglia: evidence for hemiganglionic premotor centers. Journal of Comparative Physiology A 163: 749–759.CrossRefGoogle Scholar
  25. Ryckebusch S. and Laurent G. (1993). Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. Journal of Neurophysiology 69, 1583–1595.PubMedGoogle Scholar
  26. Schmitz J., Büschges A. and Kittmann R. (1991). Intracellular recordings from nonspiking interneurons in a semi-intact, tethered walking insect. Journal of Neurobiology 22, 907–921.PubMedCrossRefGoogle Scholar
  27. Stevenson P.A. and Kutsch W. (1987). A reconsideration of the central pattern generator concept for locust flight. Journal of Comparative Physiology A 161, 115–129.CrossRefGoogle Scholar
  28. Wendler G (1985). Insect locomotory systems: control by proprioceptive and exteroceptive inputs. In: Insect locomotion eds Gewecke M. and Wendler G. 245–254. Parey Verlag, Berlin, Hamburg.Google Scholar
  29. Wilson J.A. (1979). The structure and function of serially homologous leg motor neurons in the locust. I. Anatomy. Journal of Neurobiology 10, 41–65.PubMedCrossRefGoogle Scholar
  30. Wolf H. (1990). Activity patterns of inhibitory motoneurons and their impact on leg movement in tethered walking locusts. Journal of Experimental Biology 152, 281–304.Google Scholar
  31. Wolf H. (1991). Sensory feedback in locust flight patterning. In: Locomotor neural mechanisms in arthropods and vertebrates eds Armstrong D.M. and Bush B.M.H. 134–148. Manchester University Press, Manchester, New York.Google Scholar
  32. Wolf H. (1992). Reflex modulation in locusts walking on a treadwheel — intracellular recordings from motoneurons. Journal of Comparative Physiology A 170, 443–462.CrossRefGoogle Scholar
  33. Wolf H. (1993). The locust tegula: significance for flight rhythm generation, wing movement control, and aerodynamic force production. Journal of Experimental Biology 182, 229–253.Google Scholar
  34. Wolf H. and Pearson K.G. (1988). Proprioceptive input patterns elevator activity in the locust flight system. Journal of Neurophysiology 59, 1831–1853.PubMedGoogle Scholar
  35. Wolf H., Ronacher B. and Reichert H. (1988). Patterned synaptic drive to locust flight motoneurons after hemisection of thoracic ganglia. Journal of Comparative Physiology A 163, 761–769.CrossRefGoogle Scholar
  36. Wolf H. and Laurent G.L. (1993). Rhythmic modulation of the responsiveness of locust sensory local interneurons by walking pattern generating networks. Journal of Neurophysiology 71, 110-118.Google Scholar
  37. Wolf H. and Büschges A. (1994). Insect nonspiking local interneurons and the control of leg swing in walking. In: Sensory transduction (proceedings of the 22th Göttingen neurobiology conference) eds Eisner N. and Breer H. Poster 282, Thieme Verlag, Stuttgart, New York.Google Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • H. Wolf
    • 1
  1. 1.Fakultät für BiologieUniversität KonstanzKonstanzGermany

Personalised recommendations