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Neuronal control of walking: studies on insects

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e-Neuroforum

Abstract

The control of walking in insects is to a substantial amount a function of neuronal networks in the thoracic ganglia. While descending signals from head ganglia provide general commands such as for walking direction and velocity, it is the thoracic central nervous system that controls movements of individual joints and legs. The coordination pattern of legs is velocity dependent. However, a clear stereotypic coordination pattern appears only at high velocities. In accordance with the unit burst oscillator concept, oscillatory networks (central pattern generators (CPGs)) interlocked with movement and load sensors control the timing and amplitude of joint movements. For a leg’s movements different joint CPGs of a leg are mainly coupled by proprioceptors. Differential processing of proprioceptive signals allows a task specific modulation of leg movements, for example, for changing movement direction. A switch between walking and searching movements of a leg is under local control. When stepping into a gap missing sensory input and the activation of a local command neuron evokes stereotypic searching movements of the leg.

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References

  1. Akay T, Bässler U, Gerharz P, Büschges A (2001) The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. J Neurophysiol 85:594–604

    CAS  PubMed  Google Scholar 

  2. Bässler U (1988) Functional principles of pattern generation for walking movements of stick insect forelegs: the role of the femoral chordotonal organ afferences. J Exp Biol 136:125–147

    Google Scholar 

  3. Berg E, Büschges A, Schmidt J (2013) Single perturbations cause sustained changes in searching behavior in stick insects. J Exp Biol 216:1064–1074

    Article  PubMed  Google Scholar 

  4. Berg EM, Hooper SL, Schmidt J, Büschges A (2015) A leg-local neural mechanism mediates the decision to search in stick insect. Curr Biol 25:2012–2017

    Article  CAS  PubMed  Google Scholar 

  5. Berkowitz A, Laurent G (1996) Local control of leg movements and motor patterns during grooming in locusts. J Neurosci 16:8067–8078

    CAS  PubMed  Google Scholar 

  6. Bidaye SS, Machacek C, Wu Y, Dickson BJ (2014) Neuronal control of Drosophila walking direction. Science 344:97–101

    Article  CAS  PubMed  Google Scholar 

  7. Böhm H, Schildberger K (1992) Brain neurons involved in the control of walking in the cricket Gryllus bimaculatus. J Exp Biol 166:113–130

    Google Scholar 

  8. Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, Oxford

    Book  Google Scholar 

  9. Büschges A (2005) Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. J Neurophysiol 93:1127–1135

    Article  PubMed  Google Scholar 

  10. Büschges A, Schmitz J, Bässler U (1995) Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine. J Exp Biol 198:435–456

    Google Scholar 

  11. Büschges A, Ludwar BCh, Bucher D, Schmidt J, DiCaprio RA (2004) Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system. Eur J Neurosci 19:1856–1862

  12. Büschges A, Akay T, Gabriel JP, Schmidt J (2008) Organizing network action for locomotion: insights from studying insect walking. Brain Res Rev 57:162–171

    Article  PubMed  Google Scholar 

  13. Buschmann T, Ewald A, von Twickel A, Büschges A (2015) Controlling legs for locomotion—insights from robotics and neurobiology. Bioinspir Biomim 10:041001

    Article  PubMed  Google Scholar 

  14. Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods? Trends Neurosci 13:15–21

    Article  CAS  PubMed  Google Scholar 

  15. Dürr V (2001) Stereotypic leg searching movements in the stick insect: kinematic analysis, behavioural context and simulation. J Exp Biol 204:1589–1604

    PubMed  Google Scholar 

  16. Elsner N (1974) Neuroethology of sound production in gomphocerine grasshoppers (Orthoptera: acrididae). I. Song patterns and stridulatory movements. J Comp Physiol 88:67–102

    Article  Google Scholar 

  17. Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766

    Article  CAS  PubMed  Google Scholar 

  18. Hägglund M, Dougherty KJ, Borgius L, Itohara S, Iwasato T, Kiehn O (2013) Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion. Proc Natl Acad Sci 110:11589–11594

    Article  PubMed Central  PubMed  Google Scholar 

  19. Hedwig B, Heinrich R (1997) Identified descending brain neurons control different stridulatory motor patterns in an acridid grasshopper. J Comp Physiol 180:285–294

    Article  Google Scholar 

  20. Hellekes K, Blincow E, Hoffmann J, Büschges A (2012) Control of reflex reversal in stick insect walking: effects of intersegmental signals, changes in direction, and optomotor-induced turning. J Neurophysiol 107:239–249

    Article  PubMed  Google Scholar 

  21. Knops S, Tóth TI, Guschlbauer C, Gruhn M, Daun-Gruhn S (2013) A neuromechanical model for the neuronal basis of curve walking in the stick insect. J Neurophysiol 109:679–691

    Article  CAS  PubMed  Google Scholar 

  22. Ludwar BC, Westmark S, Büschges A, Schmidt J (2005) Modulation of membrane potential in mesothoracic moto- and interneurons during stick insect front-leg walking. J Neurophysiol 94:2772–2784

    Article  PubMed  Google Scholar 

  23. Marder E, Calabrese RL (1996) Principles of rhythmic pattern generation. Physiol Rev 76:687–717

    CAS  PubMed  Google Scholar 

  24. Marek PE, Bond JE (2006) Biodiversity hotspots: rediscovery of the world’s leggiest animal. Nature 441:707

    Article  CAS  PubMed  Google Scholar 

  25. Orlovsky G, Deliagina T, Grillner S (1999) Neuronal control of locomotion. Oxford University Press, Oxford

    Book  Google Scholar 

  26. Stein PS (2008) Motor pattern deletions and modular organization of turtle spinal cord. Brain Res Rev 57:118–124

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Tóth TI, Knops S, Daun-Gruhn S (2012) A neuro-mechanical model explaining forward and backward stepping in the stick insect. J Neurophysiol 107:3267–3280

    Article  PubMed  Google Scholar 

  28. Wendler G (1965) The co-ordination of walking movements in arthropods. Symp Soc Exp Biol 20:229–249

    Google Scholar 

  29. Westmark S, Oliveira EE, Schmidt J (2009) Pharmacological analysis of tonic activity in motoneurons during stick insect walking. J Neurophysiol 102:1049–1061

    Article  CAS  PubMed  Google Scholar 

  30. Wosnitza A, Bockemühl T, Dübbert M, Scholz H, Büschges A (2013) Inter-leg coordination on the control of walking speed in Drosophila. J Exp Biol 216:480–491

    Article  PubMed  Google Scholar 

  31. Zill SN, Schmitz J, Chaudhry S, Büschges A (2012) Force encoding in stick insect legs delineates a reference frame for motor control. J Neurophysiol 108:1453–1472

    Article  PubMed Central  PubMed  Google Scholar 

  32. Zill SN, Chaudhry S, Exter A, Büschges A, Schmitz J (2014) Positive force feedback in development of substrate grip in the stick insect tarsus. Arthropod Struct Dev 43:441–455

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Till Bockemühl for reviewing and translating the text into English and Sherylane Seeliger for help with the figures. The work of the authors is supported by DFG grants Bu 857 and Schm 1084.

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Correspondence to Ansgar Büschges.

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Büschges, A., Schmidt, J. Neuronal control of walking: studies on insects. e-Neuroforum 6, 105–112 (2015). https://doi.org/10.1007/s13295-015-0017-8

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