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Journal of comparative physiology

, Volume 115, Issue 1, pp 1–27 | Cite as

Neuronal control of locomotion in the lobster,Homarus americanus

I. Motor programs for forward and backward walking
  • Joseph L. AyersJr.
  • William J. Davis
Article

Summary

  1. 1.

    Lobsters that are tethered in place on a treadmill (Fig. 3) walk against the direction of belt movement (Table 2). Forward and backward locomotion over the full range of step frequencies can be controlled by this method, even in the absence of visual input. The passive traction provided by a moving substrate is therefore an effective stimulus for walking and presumably operates in parallel with previously described optomotor pathways to provide positive feedback reinforcement of locomotory behavior.

     
  2. 2.

    The movements (Figs. 1, 6) and muscular anatomy (Fig. 2) of a lobster walking leg are described. On the basis of simultaneous extracellular recording from several leg muscles (Fig. 5), and motion picture analysis, the overall patterns of joint movement and muscular coordination underlying forward and backward walking are described (Figs. 5, 6, 7).

     
  3. 3.

    Some muscles that are synergic for forward walking are antagonistic for backward walking (Figs. 6, 7). Similarly movements that are synergic for lateral walking on the leading side are antagonistic for lateral walking on the trailing side (Fig. 6).

     
  4. 4.

    Quantitative analysis of leg movements (Fig. 9) and electromyograms (Fig. 10) have shown that the walking muscles can be subdivided into three different functional classes: return stroke muscles, which exhibit bursts of relatively constant duration irrespective of step frequency (Fig. 10A); power stroke muscles in which burst duration varies linearly with step frequency (Fig. 10B); and bifunctional muscles, which exhibit the discharge characteristics of either return or power stroke muscles, depending on the direction of walking (Fig. 10C).

     
  5. 5.

    Several lines of evidence (Table 3, Figs. 6, 7, 9, 10, 12) suggest that the limb elevator motoneurones (or their central antecedents) function as the central pacemaker of the walking system, and that other cyclic leg movements are appended to the basic elevation/depression cycle as appropriate to the direction of walking. Evidence is presented that proprioceptive inputs provided by passive traction are capable of controlling the direction of locomotion (Table 2), and determining the periodicity of stepping (Fig. 4), by altering the duration of powerstroke bursts (Figs. 9, 10, 15).

     

Keywords

Step Frequency Positive Feedback Reinforcement Return Stroke Homarus Americanus Forward Walking 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ayers, J.L., Davis, W.J.: Neuronal control of locomotion in the lobster,Homarus americanus. II. Types of walking leg reflexes. J. comp. Physiol.115, 29–46 (1977)Google Scholar
  2. Barnes, W.J.P., Spirito, C.P., Evoy, W.H.: Nervous control of walking in the crabCardisoma guanhumi. II. Role of reflexes in walking. Z. vergl. Physiol.76, 16–31 (1972)Google Scholar
  3. Bowerman, R.F., Larimer, J.L.: Command fibers in the circumoesophageal connectives of the crayfish. I. Tonic fibers. J. exp. Biol.60, 95–117 (1974a)Google Scholar
  4. Bowerman, R.F., Larimer, J.L.: Command fibers in the circumoesophageal connectives of the crayfish. II. Phasic fibers. J. exp. Biol.60, 119–134 (1974b)Google Scholar
  5. Bush, B.M.H.: Leg reflexes from chordotonal organs in the crab,Carcinus maenas. Comp. Biochem. Physiol.15, 567–587 (1965)Google Scholar
  6. Burrows, M.: Modes of activation of motoneurones controlling ventilatory movements of the locust abdomen. Phil. Trans. B269, 29–48 (1974)Google Scholar
  7. Camhi, J.M.: Neural mechanisms of response modification in insects. In: Experimental analysis of insect behavior, (L. Barton-Brown, ed.), pp. 119–134. Berlin-Heidelberg-New York: Springer 1974Google Scholar
  8. Clarac, F., Coulmance, M.: La marche latérale du crabe (Carcinus). Coordination des mouvements articulaires et régulation proprioceptive. Z. vergl. Physiol.73, 408–438 (1971)Google Scholar
  9. Clarac, F., Vedel, J.P.: Etude des relations fonctionnelles entre le muscle fléchisseur accessoire et les organes sensoriels chordotonaux et myochordotonaux des appendices locomoteurs de la langoustePalinurus vulgaris. Z. vergl. Physiol.72, 386–410 (1971)Google Scholar
  10. Clarac, F., Wales, W.: Contrôle sensoriel des muscles élévateurs au cours de la marche et de l'autotomie chez certains crustacés dédapodes. C.R. Acad. Sci. (Paris)271, 2163–2166 (1970)Google Scholar
  11. Davis, W.J.: The neural control of swimmeret beating in the lobster. J. exp. Biol.50, 99–118 (1969a)Google Scholar
  12. Davis, W.J.: Reflex organization in the swimmeret system of the lobster: I. Intrasegmental reflexes. J. exp. Biol.51, 547–563 (1969b)Google Scholar
  13. Davis, W.J.: Reflex organization in the swimmeret system of the lobster: II. Reflex dynamics. J. exp. Biol.51, 565–573 (1969c)Google Scholar
  14. Davis, W.J.: Functional significance of motoneuron size and soma position in swimmeret system of the lobster. J. Neurophysiol.34, 274–288 (1971)Google Scholar
  15. Davis, W.J.: Neuronal organization and ontogeny in the lobster swimmeret system. In: Control of posture and locomotion (R.B. Stein, K.G. Pearson, R.S. Smith, J.B. Redford, eds.), pp. 437–455. New York: Plenum Press 1973Google Scholar
  16. Davis, W.J.: Organizational concepts in the central motor networks of invertebrates. In: Neural control of locomotion (R. Herman, S. Grillner, P.S.G. Stein, D. Stuart, eds.), pp. 265–292. New York: Plenum Press 1976Google Scholar
  17. Davis, W.J., Ayers, J.L.: Locomotion: control by positive feedback optokinetic responses. Science177, 183–185 (1972)Google Scholar
  18. Davis, W.J., Kennedy, D.: Command interneurons controlling swimmeret movements in the lobster. I. Types of effects on motoneurons. J. Neurophysiol.35, 1–12 (1972a)Google Scholar
  19. Davis, W.J., Kennedy, D.: Command interneurons controlling swimmeret movements in the lobster. II. Interaction of effects on motoneurons. J. Neurophysiol.35, 13–19 (1972b)Google Scholar
  20. Delcomyn, F., Davis, W.J.: 360 biological reflex program: computer program for cross-correlation between digital bioelectric output and sinusoidal and step inputs. SHARE contribution No. 360-17.5.001. SHARE Program Library Agency, COSMIC-Barrow Hall, University of Georgia, Athens, Ga. 30601 (1968)Google Scholar
  21. Elsner, N.: Neural economy: Bifunctional muscles and common central pattern elements in leg and wing stridulation in the grasshopperStenobothrus rubicundus Germ. J. comp. Physiol.89, 227–236 (1974)Google Scholar
  22. Evoy, W.J., Fourtner, C.R.: Nervous control of walking in the crabCardisoma guanhumi. III. Proprioceptive influences on intra- and intersegmental coordination. J. comp. Physiol.83, 303–318 (1973)Google Scholar
  23. Grillner, S.: Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol. Rev.55, 247–304 (1975)Google Scholar
  24. Gurfinkel, V.S., Shik, M.S.: The control of posture and locomotion. In: Motor control (A.A. Gydikov, N.T. Tankov, D.S. Kosarov eds.). New York: Plenum Press 1973Google Scholar
  25. Hughes, G.M.: The coordination of insect movements, the effects of limb amputation and the cutting of commissures in the cockroach,Blatta orientalis. J. exp. Biol.34, 306–333 (1957)Google Scholar
  26. Herman, R.E., Grillner, S., Stein, P., Stuart, D., (eds.): Proceedings of the International Conference on Neural Control of Locomotion. New York: Plenum Press 1976Google Scholar
  27. Kennedy, D., Calabrese, R., Wine, J.: Presynaptic inhibition: primary afferent depolarization in crayfish neurons. Science186, 451–454 (1975)Google Scholar
  28. Kennedy, D., Davis, W.J.: The organization of invertebrate motor systems. In: Handbook of Physiology, vol. 2, Neurophysiology (E.R. Kandel, ed.) second edition. Bethesda: Amer. physiol. Soc. (in press)Google Scholar
  29. Krasne, F.G., Bryan, J.S.: Habituation: regulation through presynaptic inhibition. Science182, 590–592 (1973)Google Scholar
  30. MacLeese, D.W., Wilder, D.G.: The activity and catchability of the lobsterHomarus americanus in relation to temperature. J. Fish. Res. Brd. Canada1, 1345–1359 (1958)Google Scholar
  31. MacMillan, D.L.: A physiological analysis of walking in the American lobster,Homarus americanus. Phil. Trans. B270, 1–59 (1975)Google Scholar
  32. Miller, S., Van der Berg, J., Van der Meché, F.G.A.: Locomotion in the cat: Basic programmes of movement. Brain Res.91, 239–253 (1975)Google Scholar
  33. Orlovskii, G.N., Severin, F. W., Shik, M.L.: Effect of speed and load on coordination of movements during running of the dog. Biofizika11, 414–417 (1966)Google Scholar
  34. Orlovskii, G.N., Shik, M.L.: Standard elements of cyclic movements. Biofizika10, 847–854 (1965)Google Scholar
  35. Pearson, K.G.: Central programming and reflex control of walking in the cockroach. J. exp. Biol.56, 173–193 (1972)Google Scholar
  36. Perkel, D.H., Mulloney, B.: Motor pattern production in reciprocally inhibitory neurones exhibiting post-inhibitory rebound. Science185, 181–183 (1974)Google Scholar
  37. Sandeman, D.C.: A sensitive position measuring device for biological systems. Comp. Biochem. Physiol.24, 635–638 (1968)Google Scholar
  38. Schmidt, W.: Die Muskulatur vonAstacus fluviatilis (Potambius astacus L.). Ein Beitrag zur Morphologie der Decapoden. Z. wiss. Zool.113, 165–251 (1915)Google Scholar
  39. Scrivener, J.C.E.: Agonistic behavior of the American lobsterHomarus americanus. Fish. Res. Bd. Canada Tech. Rept. No. 235 (1971)Google Scholar
  40. Selverston, A.I., King, D.G., Russel, D.F., Miller, J.P.: The stomatogastric nervous system: structure and function of a small neural network. Progr. Neurobiol.7, 215–290 (1976)Google Scholar
  41. Severin, F.V., Shik, M.L., Orlovskii, G.N.: Work of the muscles and single motoneurones during controlled locomotion. Biofizika12, 762–772 (1967)Google Scholar
  42. Shik, M.L., Severin, F.V., Orlovskii, G.N.: Control of walking and running by means of electrical stimulation of the midbrain. Biofizika11, 659 (1966)Google Scholar
  43. Siegler, M.V.S., Mpitsos, G.J., Davis, W.J.: Motor organization and generation of rhythmic feeding output in the buccal ganglion ofPleurobranchaea. J. Neurophysiol.37, 1173–1196 (1974)Google Scholar
  44. Snodgrass, R.E.: A textbook of arthropod anatomy. Ithaca, N.Y.: Cornell Univ. Press 1952Google Scholar
  45. Spira, M.E., Bennett, M.V.L.: Synaptic control of electrotonic coupling between neurons. Brain Res.37, 294–300 (1972)Google Scholar
  46. Spirito, C.P., Evoy, W.H., Fourtner, C.R.: Consideration of proprioception and neuromuscular integration in Crustacean locomotion. Amer. Zool.13, 427–434 (1973)Google Scholar
  47. Ten Cate, J.: Beiträge zur Innervation der Lokomotionsbewegung der Heuschrecke (Locusta viridissima). Arch. néed. Physiol.21, 562–566 (1938)Google Scholar
  48. Wales, W., Clarac, F., Dando, M.R., Laverack, M.S.: Innervation of the receptors present at the various joints of the periopods and third maxilliped ofHomarus gammarus and other Macruran decapods. Z. vergl. Physiol.68, 345–384 (1970)Google Scholar
  49. Ward, J.: Some notes on the physiology of the freshwater crayfish (Astacus fluviatilis). J. Physiol. (Lond.)2, 214–227 (1879)Google Scholar
  50. Wendler, G.: The coordination of walking movements in arthropods. Symp. Soc. exp. Biol.20, 229–249 (1966)Google Scholar
  51. Wilson, D.M.: Bifunctional muscles in the thorax of grasshoppers. J. exp. Biol.39, 669–677 (1962)Google Scholar
  52. Wilson, D.M., Gettrup, E.: A stretch reflex controlling wingbeat frequency in grasshoppers. J. exp. Biol.40, 171–185 (1963)Google Scholar
  53. Wyse, G., Dwyer, N.K., The neuromuscular basis of coxal feeding and locomotory movements inLimulus. Biol. Bull.144, 567–579 (1973)Google Scholar

Copyright information

© Springer-Verlag 1977

Authors and Affiliations

  • Joseph L. AyersJr.
    • 1
  • William J. Davis
    • 1
  1. 1.The Thimann LaboratoriesUniversity of CaliforniaSanta CruzUSA

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