Summary
-
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.
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.
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.
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.
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).
Similar content being viewed by others
References
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)
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)
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)
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)
Bush, B.M.H.: Leg reflexes from chordotonal organs in the crab,Carcinus maenas. Comp. Biochem. Physiol.15, 567–587 (1965)
Burrows, M.: Modes of activation of motoneurones controlling ventilatory movements of the locust abdomen. Phil. Trans. B269, 29–48 (1974)
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 1974
Clarac, F., Coulmance, M.: La marche latérale du crabe (Carcinus). Coordination des mouvements articulaires et régulation proprioceptive. Z. vergl. Physiol.73, 408–438 (1971)
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)
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)
Davis, W.J.: The neural control of swimmeret beating in the lobster. J. exp. Biol.50, 99–118 (1969a)
Davis, W.J.: Reflex organization in the swimmeret system of the lobster: I. Intrasegmental reflexes. J. exp. Biol.51, 547–563 (1969b)
Davis, W.J.: Reflex organization in the swimmeret system of the lobster: II. Reflex dynamics. J. exp. Biol.51, 565–573 (1969c)
Davis, W.J.: Functional significance of motoneuron size and soma position in swimmeret system of the lobster. J. Neurophysiol.34, 274–288 (1971)
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 1973
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 1976
Davis, W.J., Ayers, J.L.: Locomotion: control by positive feedback optokinetic responses. Science177, 183–185 (1972)
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)
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)
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)
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)
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)
Grillner, S.: Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol. Rev.55, 247–304 (1975)
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 1973
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)
Herman, R.E., Grillner, S., Stein, P., Stuart, D., (eds.): Proceedings of the International Conference on Neural Control of Locomotion. New York: Plenum Press 1976
Kennedy, D., Calabrese, R., Wine, J.: Presynaptic inhibition: primary afferent depolarization in crayfish neurons. Science186, 451–454 (1975)
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)
Krasne, F.G., Bryan, J.S.: Habituation: regulation through presynaptic inhibition. Science182, 590–592 (1973)
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)
MacMillan, D.L.: A physiological analysis of walking in the American lobster,Homarus americanus. Phil. Trans. B270, 1–59 (1975)
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)
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)
Orlovskii, G.N., Shik, M.L.: Standard elements of cyclic movements. Biofizika10, 847–854 (1965)
Pearson, K.G.: Central programming and reflex control of walking in the cockroach. J. exp. Biol.56, 173–193 (1972)
Perkel, D.H., Mulloney, B.: Motor pattern production in reciprocally inhibitory neurones exhibiting post-inhibitory rebound. Science185, 181–183 (1974)
Sandeman, D.C.: A sensitive position measuring device for biological systems. Comp. Biochem. Physiol.24, 635–638 (1968)
Schmidt, W.: Die Muskulatur vonAstacus fluviatilis (Potambius astacus L.). Ein Beitrag zur Morphologie der Decapoden. Z. wiss. Zool.113, 165–251 (1915)
Scrivener, J.C.E.: Agonistic behavior of the American lobsterHomarus americanus. Fish. Res. Bd. Canada Tech. Rept. No. 235 (1971)
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)
Severin, F.V., Shik, M.L., Orlovskii, G.N.: Work of the muscles and single motoneurones during controlled locomotion. Biofizika12, 762–772 (1967)
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)
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)
Snodgrass, R.E.: A textbook of arthropod anatomy. Ithaca, N.Y.: Cornell Univ. Press 1952
Spira, M.E., Bennett, M.V.L.: Synaptic control of electrotonic coupling between neurons. Brain Res.37, 294–300 (1972)
Spirito, C.P., Evoy, W.H., Fourtner, C.R.: Consideration of proprioception and neuromuscular integration in Crustacean locomotion. Amer. Zool.13, 427–434 (1973)
Ten Cate, J.: Beiträge zur Innervation der Lokomotionsbewegung der Heuschrecke (Locusta viridissima). Arch. néed. Physiol.21, 562–566 (1938)
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)
Ward, J.: Some notes on the physiology of the freshwater crayfish (Astacus fluviatilis). J. Physiol. (Lond.)2, 214–227 (1879)
Wendler, G.: The coordination of walking movements in arthropods. Symp. Soc. exp. Biol.20, 229–249 (1966)
Wilson, D.M.: Bifunctional muscles in the thorax of grasshoppers. J. exp. Biol.39, 669–677 (1962)
Wilson, D.M., Gettrup, E.: A stretch reflex controlling wingbeat frequency in grasshoppers. J. exp. Biol.40, 171–185 (1963)
Wyse, G., Dwyer, N.K., The neuromuscular basis of coxal feeding and locomotory movements inLimulus. Biol. Bull.144, 567–579 (1973)
Author information
Authors and Affiliations
Additional information
We thank Dr. F. Clarac, Dr. D. Kennedy, Dr. K.G. Pearson and Dr. A.I. Selverston for comments on previous drafts of this manuscript and Wm. Nichparenko for designing the multiplexing system and transducers. Supported by NIH Research Grant NS 09050 to W.J.D.
Rights and permissions
About this article
Cite this article
Ayers, J.L., Davis, W.J. Neuronal control of locomotion in the lobster,Homarus americanus . J. Comp. Physiol. 115, 1–27 (1977). https://doi.org/10.1007/BF00667782
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00667782