Abstract
Few studies in arthropods have documented to what extent local control centers in the thorax can support locomotion in absence of inputs from head ganglia. Posture, walking, and leg motor activity was examined in cockroaches with lesions of neck or circumoesophageal connectives. Early in recovery, cockroaches with neck lesions had hyper-extended postures and did not walk. After recovery, posture was less hyper-extended and animals initiated slow leg movements for multiple cycles. Neck lesioned individuals showed an increase in walking after injection of either octopamine or pilocarpine. The phase of leg movement between segments was reduced in neck lesioned cockroaches from that seen in intact animals, while phases in the same segment remained constant. Neither octopamine nor pilocarpine initiated changes in coordination between segments in neck lesioned individuals. Animals with lesions of the circumoesophageal connectives had postures similar to intact individuals but walked in a tripod gait for extended periods of time. Changes in activity of slow tibial extensor and coxal depressor motor neurons and concomitant changes in leg joint angles were present after the lesions. This suggests that thoracic circuits are sufficient to produce leg movements but coordinated walking with normal motor patterns requires descending input from head ganglia.
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Abbreviations
- SOG:
-
Suboesophageal ganglion
- NL:
-
Neck connective lesion
- CoCL:
-
Circumoesophageal connective lesion
- Ds:
-
Slow depressor of the trochanter motor neuron
- SETi:
-
Slow extensor of the tibia motor neuron
- Fti:
-
Femur- tibia joint
- CTr:
-
Coxa- trochanter joint
References
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
Altman JS, Kien J (1979) Suboesophageal neurons involved in head movements and feeding in locusts. Proc R Soc Lond B Biol Sci 205:209–227
Altman JS, Kien J (1987) Functional organization of the subesophageal ganglion in arthropods. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and function. Wiley, New York, p 588
Barbeau H, Norman KE (2003) The effect of noradrenergic drugs on the recovery of walking after spinal cord injury. Spinal Cord 41:137–143
Barbeau H, Rossignol S (1987) Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412:84–95
Barbeau H, Chau C, Rossignol S (1993) Noradrenergic agonists and locomotor training affect locomotor recovery after cord transection in adult cats. Brain Res Bull 30:387–393
Bässler U, Büschges A (1998) Pattern generation for stick insect walking movements-multisensory control of a locomotor program. Brain Res Rev 27:65–88
Belanger M, Drew T, Provencher J, Rossignol S (1996) A comparison of treadmill locomotion in adult cats before and after spinal transection. J Neurophysiol 76:471–491
Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobio 63:441–466
Büschges A, Schmitz J, Bässler U (1995) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Exp Biol 198:435–456
Chau C, Barbeau H, Rossignol S (1998a) Effects of intrathecal alpha1- and alpha2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. J Neurophysiol 79:2941–2963
Chau C, Barbeau H, Rossignol S (1998b) Early locomotor training with clonidine in spinal cats. J Neurophysiol 79:392–409
Comer CM, Robertson RM (2001) Identified nerve cells and insect behavior. Prog Neurobio 63:409–439
Comer CM, Parks L, Halvorsen MB, Breese-Terteling A (2003) The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions. J Comp Physiol A 189:97–103
Cruse H (1976) The function of legs in the free walking stick insect, Carausius morosus. J Comp Physiol A 112:135–162
Cruse H (1985) Coactivating influences between neighbouring legs in walking insects. J Exp Biol 114:513–519
Cruse H, Schwarze W (1988) Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus). J Exp Biol 138:455–469
Dasari S, Cooper RL (2004) Modulation of sensoryCNSmotor circuits by serotonin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227
De Leon R, Hodgson J, Roy R, Edgerton V (1998a) Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol 79:1329–1340
De Leon RD, Hodgson JA, Roy RR, Edgerton VR (1998b) Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J Neurophysiol 80:83–91
De Leon RD, Hodgson JA, Roy RR, Edgerton VR (1999) Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J Neurophysiol 81:85–94
Delcomyn F (1971) Locomotion of the cockroach Periplaneta americana. J Exp Biol 54:443–452
Drew T (1988) Motor cortical cell discharge during voluntary gait modification. Brain Res 457:181–187
Drew T (1993) Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. J Neurophysiol 70:179–199
Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251–261
El Manira A, Pombal MA, Grillner S (1997) Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389:603–616
Foth E, Bässler U (1985) Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor-driven belt. Biol Cyber 51:319–324
Full RJ, Tu MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156:215–231
Giroux N, Chau C, Barbeau H, Reader TA, Rossignol S (2003) Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats. J Neurophysiol 90:1027–1045
Graham D (1979) Effects of circum-oesophageal lesion on the behaviour of the stick insect, Carausius morosus. II. Changes in walking co-ordination. Biol Cyber 32:147–152
Grillner S (1997) Ion channels and locomotion. Science 278:1087–1088
Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573–586
Grillner S, Deliagina T, Ekeberg O, el Manira A, Hill RH, Lansner A, Orlovsky GN, Wallen P (1995) Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci 18:270–279
Grillner S, Cangiano L, Hu G-Y, Thompson R, Hill R, Wallen P (2000) The intrinsic function of a motor system-from ion channels to networks and behavior. Brain Res 886:224–236
Hiebert GW, Pearson KG (1999) Contribution of sensory feedback to the generation of extensor activity during walking in the decerebrate cat. J Neurophysiol 81:758–770
Horseman BG, Gebhardt MJ, Honnegger HW (1997) Involvement of the suboesophageal and thoracic ganglia in the control of antennal movements in the cricket. J Comp Physiol A 181:195–204
Jindrich DL, Full RJ (1999) Many-legged maneuverability: dynamics of turning in hexapods. J Exp Biol 202:1603–1623
Johnston RM, Levine RB (1996) Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. J Neurophysiol 76:3178–3195
Johnston RM, Consoulas C, Pflüger H, Levine RB (1999) Patterned activation of unpaired median neurons during fictive crawling in manduca sexta larvae. J Exp Biol 202(Pt 2):103–113
Kiehn O, Eken T (1997) Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? J Neurophysiol 78:3061–3068
Kien J (1983) The initiation and maintenance of walking in the locust: an alternative to the command concept. Proc R Soc Lond B Biol Sci 219:137–174
Kien J, Altman J (1992) Preparation and execution of movement: parallels between insects and mammalian motor systems. Comp Biochem Physiol 103A:15–24
Kozlov AK, Ullen F, Fagerstedt P, Aurell E, Lansner A, Grillner S (2002) Mechanisms for lateral turns in lamprey in response to descending unilateral commands: a modeling study. Biol Cybern 86:1–14
Lovely RG, Gregor RJ, Roy RR, Edgerton VR (1986) Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol 92:421–435
McLean DL, Sillar KT (2003) Spinal and supraspinal functions of noradrenaline in the frog embryo: consequences for motor behaviour. J Physiol 551:575–587
Neter J, Kutner M, Nachtsheim C, Wasserman W (1996) Applied linear statistical models. The McGraw-Hill Companies Inc., Boston MA
Noah JA, Quimby L, Frazier SF, Zill SN (2001) Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered. J Comp Physiol A 187:769–784
Noah JA, Quimby L, Frazier SF, Zill SN (2004) Walking on a ’peg leg’: extensor muscle activities and sensory feedback after distal leg denervation in cockroaches. J Comp Physiol A 190:217–231
Pearson K, Fourtner C (1975) Nonspiking interneurons in the walking system of the cockroach. J Neurophysiol 38:33–52
Pearson K, Iles J (1970) Discharge patters of the coxal levators and depressor motorneurons of the cockroach. J Exp Biol 52:139–165
Pombal MA, Marin O, Gonzalez A (2001) Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain. J Comp Neurol 431:105–126
Quinlan KA, Placas PG, Buchanan JT (2004) Cholinergic modulation of the locomotor network in the lamprey spinal cord. J Neurophysiol 92:1536–1548
Ridgel AL, Frazier SF, Zill SN (2001) Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches. J Comp Physiol A 187:405–420
Ritzmann RE, Pollack AJ, Archinal J, Ridgel AL, Quinn RD (2005) Descending control of body attitude in the cockroach, Blaberus discoidalis and its role in incline climbing. J Comp Physiol A 191:253–264
Roeder K (1937) The control of tonus and locomotor activity in the praying mantis (Mantis religiosa L.). J Exp Biol 76:353–374
Rossignol A (1996) Neural control of stereotypical limb movements. In: Handbook of Physiology. Exercise: Regulation and integration of multiple systems. American Physiological Society, Bethesda, pp 173–216
Rossignol S, Chau C, Brustein E, Belanger M, Barbeau H, Drew T (1996) Locomotor capacities after complete and partial lesions of the spinal cord. Acta Neurobiol Exp (Wars) 56:449–463
Ryckebusch S, Laurent G (1993) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Neurophysiol 69:1583–1595
Schaefer P, Ritzmann R (2001) Descending influences on escape behavior and motor pattern in the cockroach. J Neurobio 49:9–28
Selverston A (1999) What invertebrate circuits have taught us about the brain. Brain Res Bull 50:439–440
Tryba AK, Ritzmann RE (2000a) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. J Neurophysiol 83:3323–3336
Tryba AK, Ritzmann RE (2000b) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern. J Neurophysiol 83:3337–3350
Wallen P, Williams TL (1984) Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. J Physiol 347:225–239
Wang H, Jung R (2002) Variability analyses that supraspino-spinal interactions provide dynamic stability in motor control. Brain Res 930:83–100
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, Zill SN, Pollack AJ (2002) Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics. J Comp Physiol A 188:39–53
Wilson DM (1966) Insect walking. Ann Rev Entomol 11:103–122
Zhang W, Grillner S (2000) The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey. Brain Res 879:188–192
Zill SN, Moran DT, Varela FG (1981) The exoskeleton and insect proprioception. II. Reflex effects of the tibial campaniform sensilla in the American cockroach. J Exp Biol 94:43–55
Acknowledgements
Special thanks to S.N. Zill and A.J. Pollack for their advice and help on this project. We would also like to thank Dr. Mark Willis and two anonymous reviewers for helpful comments on the manuscript. This work was supported by NIH Grant NRSA F32-NS43004 to ALR and Eglin AFB Grant F08630-01-C-0023 to RER.
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Ridgel, A.L., Ritzmann, R.E. Effects of neck and circumoesophageal connective lesions on posture and locomotion in the cockroach. J Comp Physiol A 191, 559–573 (2005). https://doi.org/10.1007/s00359-005-0621-0
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DOI: https://doi.org/10.1007/s00359-005-0621-0
Keywords
- Brain
- Suboesophageal ganglion
- Walking
- Arthropod
- Descending control