Abstract
To examine how walking patterns are adapted to changes in load, we recorded leg movements and muscle activities when cockroaches (Periplaneta americana) walked upright and on an inverted surface. Animals were videotaped to measure the hindleg femoro-tibial joint angle while myograms were taken from the tibial extensor and flexor muscles. The joint is rapidly flexed during swing and extended in stance in upright and inverted walking. When inverted, however, swing is shorter in duration and the joint traverses a range of angles further in extension. In slow upright walking, slow flexor motoneurons fire during swing and the slow extensor in stance, although a period of co-contraction occurs early in stance. In inverted walking, patterns of muscle activities are altered. Fast flexor motoneurons fire both in the swing phase and early in stance to support the body by pulling the animal toward the substrate. Extensor firing occurs late in stance to propel the animal forward. These findings are discussed within the context of a model in which stance is divided into an early support and subsequent propulsion phase. We also discuss how these changes in use of the hindleg may represent adaptations to the reversal of the effects of gravity.
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References
Bässler U (1993) The walking(and searching-) pattern generator of stick insects, a modular system composed of reflex chains and endogenous oscillators. Biol Cybern 69: 305–317
Burrows M, Laurent G (1993) Synaptic potentials in the central terminals of locust proprioceptive afferents generated by other afferents from the same sense organ. J Neurosci 13: 808–819
Büschges A, Kittmann R, Schmitz J (1994) Identified nonspiking interneurons in leg reflexes and during walking in the stick insect. J Comp Physiol A 174: 685–700
Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods? Trends Neurosci 13: 15–21
Delcomyn F (1980) Neural basis of rhythmic behavior in animals Science 210: 492–498
Delcomyn F (1987) Motor activity during searching and walking movements of cockroach legs. J Exp Biol 133: 111–120
Delcomyn F (1991a) Perturbation of the motor system in freely walking cockroaches. I. Rear leg amputation and the timing of motor activity in leg muscles. J Exp Biol 156: 483–502
Delcomyn F (1991b) Perturbation of the motor system in freely walking cockroaches. II. The timing of motor activity in leg muscles after amputation of a middle leg. J Exp Biol 156: 503–517
Dietz V, Horstmann GA, Berger W (1989) Interlimb coordination of leg-muscle activation during perturbation of stance in humans. J Neurophysiol 62: 680–693
Diggle PJ (1990) Time series, a biostatistical introduction. Clarendon Press, Oxford
El Manira A, Clarac F (1991) GABA-mediated presynaptic inhibition in crayfish primary afferents by non-A, non-B GABA receptors. Eur J Neurosci 3: 1208–1218.
Ewing AW, Manning A (1966) Some aspects of the efferent control of walking in three cockroach species. J Insect Physiol 12: 1115–1118.
Field LH, Coles MML (1994) The position-dependent nature of postural resistance reflexes in the locust. J Exp Biol 188: 65–88
Forssberg H (1979) Stumbling corrective reaction: a phase dependent compensatory reaction during locomotion. J Neurophysiol 42: 936–953.
Gauthier L, Rossignol S (1981) Contralateral hindlimb responses to cutaneous stimulation during locomotion in high decerebrate cats. Brain Res 207: 303–320
Gossard J-P, Rossignol S (1990) Phase-dependent modulation of dorsal root potentials evoked by peripheral nerve stimulation during fictive locomotion in the cat. Brain Res 537: 1–13
Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interactions. Physiol Rev 55: 247–304
Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228: 143–149
Hoyle G (1976) Arthropod walking. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds.) Neural control of locomotion. Plenum Press, New York, pp 137–177
Hughes GM (1952) The coordination of insect movements. I. The walking movements of insects. J Exp Biol 29: 267–284
Krauthamer V, Fourtner CR (1978) Locomotory activity in the extensor and flexor tibiae of the cockroach, Periplaneta americana. J Insect Physiol 24: 813–819
Libersat F, Clarac F, Zill SN (1987) Force-sensitive mechanoreceptors of the dactyl of the crab: single-unit responses during walking and evaluation of function. J Neurophysiol 57: 1618–1637
Loeb GE, Duysens J (1979) Activity patterns in individual hindlimb primary and secondary muscle spindles afferents during normal movements in unrestrained cats. J Neurophysiol 42: 420–440
Nashner LM (1980) Balance adjustments of humans perturbed when walking. J Neurophysiol 44: 650–664
Pearson KG (1972) Central programming and reflex control of walking in the cockroach. J Exp Biol 56: 173–193
Pearson KG, Fourtner CR (1975) Nonspiking interneurons in walking system of the cockroach. J Neurophysiol 38: 33–52
Pearson KG, Franklin R (1984) Characteristics of leg movements and patterns of coordination in locusts walking on rough terrain. Int J Robotics Res 3: 101–112
Pearson KG, Iles JF (1970) Discharge patterns of coxal levator and depressor motoneurones of the cockroach, Periplaneta americana. J Exp Biol 52: 139–165
Prochazka A, Wand P (1980) Tendon organ discharge during voluntary movements in cats. J Physiol 303: 385–390
Reingold S, Camhi JM (1977) A quantitative analysis of rhythmic leg movements during three different behaviors in the cockroach Periplaneta americana. J Insect Physiol 12: 1255–1263
Rossignol S, Saltiel P, Perreault M-C, Drew T, Pearson K, Belanger M (1993) Intralimb and interlimb coordination during real and fictive rhythmic motor programs Sem Neurosci 5: 67–75
Ryckebusch S, Laurent G (1993) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Neurophysiol 69: 1583–1595
Schmitz J (1993) Load-compensating reactions in the proximal leg joints of stick insects during standing and walking. J Exp Biol 183: 15–33
Tang TP, MacMillan DL (1986) The effects of sensory manipulation upon interlimb coordination during fast walking in the cockroach. J Exp Biol 125: 107–117
Zill SN (1985) Proprioceptive feedback and the control of cockroach walking. In: Barnes WJP, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates. Croom Helm, London, pp 187–208
Zill SN (1986) A model of pattern generation of cockroach walking reconsidered. J Neurobiol 17: 317–328
Zill SN (1993) Mechanisms of load compensation in insects: swaying and stepping strategies in posture and locomotion. In: Beer R, Ritzmann R, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press San Diego, California, pp 43–68
Zill SN, Moran DT (1981) The exoskeleton and insect proprioception. III. Activity of tibial campaniform sensilla during walking in the American cockroach, Periplaneta americana. J Exp Biol 94: 57–75
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Larsen, G.S., Frazier, S.F., Fish, S.E. et al. Effects of load inversion in cockroach walking. J Comp Physiol A 176, 229–238 (1995). https://doi.org/10.1007/BF00239925
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DOI: https://doi.org/10.1007/BF00239925