Walking on a ‘peg leg’: extensor muscle activities and sensory feedback after distal leg denervation in cockroaches

Zeitschrift für vergleichende Physiologie - Tập 190 - Trang 217-231 - 2004
J. A. Noah1, L. Quimby1, S. F. Frazier1, S. N. Zill1
1Department of Anatomy, Cell and Neurobiology, Marshall University School of Medicine, Huntington, USA

Tóm tắt

Previous studies in insects demonstrated that leg coordination changes following complete ablation of distal limb segments. However, normal coordination was restored when small ‘peg leg’ prostheses were attached to leg stumps to permit substrate contact. We have adapted this paradigm to preserve appropriate leg mass and inertia by severing all nerves and muscle tendons in the femur of the cockroach hind leg and converting the animal’s own limb into a peg leg. Recordings of muscle activities and leg movements before and after denervation showed that: (1) the ‘peg leg’ is actively used in walking and regular bursts occur in motoneurons to leg extensor muscles; (2) driving of motoneuron activity is sufficient to produce ‘fictive’ bursting in a muscle whose tendon (apodeme) is cut in the ablation; and (3) similar motoneuron activities are found in walking on an oiled glass surface, when the effects of body weight and mechanical coupling are minimized. When distal segments were completely severed in these preparations, leg use and muscle bursting were disrupted but could be restored if the stumps were pressed against the substrate. These results support the hypothesis that feedback from receptors in proximal leg segments indicating forces allows for active leg use in walking.

Tài liệu tham khảo

Akay T (2002) The role of sensory signals for interjoint coordination in stick insect legs (Carausius morosus and Cuniculina impigra). Doctoral dissertation, University of Koln, Germany 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 Bässler U (1977) Sensory control of leg movement in the stick insect Carausius morosus. Biol Cybern 25:61–72 Brodfuehrer P, Fourtner CR (1983) Reflexes evoked by the femoral and coxal chordotonal organs in the cockroach, Periplaneta americana. Comp Biochem Physiol 74A:169–174 Buddenbrock W von (1921) Der Rhythmus der Schreitbewegungen der Stabheuschrecke Dyxippus. Biol Zentralbl 41:41–48 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 Cruse H (1983) The influence of load and leg amputation upon coordination in walking crustaceans: a model calculation. Biol Cybern 49:119–125 Cruse H, Schmitz J, Braun U, Schweins A (1993) Control of body height in a stick insect walking on a treadwheel. J Exp Biol 181:141–155 Delcomyn F (1985) Walking and running. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 5. Nervous system: structure and motor function. Pergamon Press, Oxford, pp 439–466 Delcomyn F (1987) Motor activity during searching and walking movements of cockroach legs. J Exp Biol 133:111–120 Delcomyn F (1988) Motor activity in the stump of an amputated leg during free walking in cockroaches. J Exp Biol 140:465–476 Delcomyn F (1990a) 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 (1990b) 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 Dresden D, Nijenhuis ED (1958) Fiber analysis of the nerves of the second thoracic leg in Periplaneta americana. Proc K Ned Akad Wet C58:213–223 Duysens J, Clarac F, Cruse H (2000) Load regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80:83–133 Epstein S, Graham D (1983) Behaviour and motor output of stick insects walking on a slippery surface. I. Forward walking. J Exp Biol 105:215–229 Full RJ, Ahn AN (1995) Static forces and moments generated in the insect leg: comparison of a three-dimensional musculo-skeletal computer model with experimental measurements. J Exp Biol 198:1285–1298 Gabriel JP, Scharstein H, Schmidt J and Büschges A (2004) Control of flexor motoneuron activity during single leg walking of the stick insect on an electronically controlled treadwheel. J Neurobiol 52:237–251 Guthrie DM (1967) Multipolar stretch receptors and the insect leg reflex. J Insect Physiol 13:1637–1644 Harkema SJ, Hurley SL, Uday KP, Requejo PS, Dobkin BH, Edgerton VR (1997) Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 77:797–811 Hughes GM (1952) The coordination of insect movements. I. The walking movements of insects. J Exp Biol 29:267–284 Hughes GM (1957) The coordination of insect movements. II. The effect of limb amputation and the cutting of commissures in the cockroach (Blatta orientalis). J Exp Biol 34:306–333 Krauthamer V, Fourtner CR (1978) Locomotory activity in the extensor and flexor tibiae of the cockroach, Periplaneta americana. J Insect Physiol 24:813–819 Larsen GS, Frazier SF, and Zill SN (1997) The tarso-pretarsal chordotonal organ as an element in cockroach walking. J Comp Physiol A 180:683–700 Niederegger S, Gorb S (2003) Tarsal movement in flies during leg attachment and detachment on a smooth surface. J Insect Physiol 49:611–620 Nijenhuis ED, Dresden D (1952) A micro-morphological study of the sensory supply of the mesothoracic leg of the American cockroach, Periplaneta americana. Proc K Ned Akad Wet C55:300–310 Nijenhuis ED, Dresden D (1956) On the topographical anatomy of the nervous system of the mesothoracic leg of the American cockroach, Periplaneta americana. Proc K Ned Akad Wet C58:121–130 Noah JA, Quimby L, Frazier SF, Zill SN (2001) Force receptors in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered. J Comp Physiol A 187:769–784 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, Iles JF (1973) Nervous mechanisms underlying intersegmental co-ordination of leg movements during walking in the cockroach. J Exp Biol 58:725–744 Pearson KG, Wong RKS, Fourtner CR (1976) Connexions between hair-plate afferents and motoneurons in the cockroach leg. J Exp Biol 64:251–266 Prochazka A (1996) Proprioceptive feedback and equilibrium. In: Rowell L, Shepard J (eds) Handbook of physiology, sect 12. Oxford University Press, New York, pp 89–128 Steel J (1979) Intersegmental coordination of walking in the cockroach, Periplaneta americana. Master’s thesis, Department of Physiology, University of Alberta Ting LH, Raasch CC, Brown DA, Kautz SA, Zajac FE (1998) Sensorimotor state of contralateral leg affects ipsilateral muscle coordination of pedaling. J Neurophysiol 80:1341–1351 Tryba AK, Ritzmann RE (2000) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. J Neurophysiol 83:3323–3336 Watson JT, Ritzmann RE (1998) Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis. I. Slow Running. J Comp Physiol A 182:11–22 Watson JT, Ritzmann RE, Pollack AJ (2002) Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement. J Comp Physiol A 188:55–69 Wendler G (1964) Laufen und Stehen der Stabheuschrecke Carausius morosus: Sinnesborstenfelder in den Beingelenken als Glieder von Regelkreisen. Z Vergl Physiol 48:198–250 Wendler G (1966) The co-ordination of walking movements in arthropods. In: Nervous and Hormonal Mechanisms of Integration. Symp Soc Exp Biol 20:229–249 Wetzel MC, Atwater AE, Wait JV, Stuart DG (1976) Kinematics of locomotion by cats with a single hindlimb deafferented. J Neurophysiol 39:667–678 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 (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, 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 Zill SN, Frazier SF, MacFarland DL, Fish SE (1993) Characterization of insect sense organs and optical clearing of whole mount preparations using diI in fixed tissues. J Exp Biol 175:299–303 Zill SN, Ridgel AL, DiCaprio RA, Frazier SF (1999) Load signaling by cockroach trochanteral campaniform sensilla. Brain Res 822:271–275