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Effects of neck and circumoesophageal connective lesions on posture and locomotion in the cockroach

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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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Barbeau H, Norman KE (2003) The effect of noradrenergic drugs on the recovery of walking after spinal cord injury. Spinal Cord 41:137–143

    Article  CAS  PubMed  Google Scholar 

  • Barbeau H, Rossignol S (1987) Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412:84–95

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bässler U, Büschges A (1998) Pattern generation for stick insect walking movements-multisensory control of a locomotor program. Brain Res Rev 27:65–88

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Buchanan JT (2001) Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog Neurobio 63:441–466

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Chau C, Barbeau H, Rossignol S (1998b) Early locomotor training with clonidine in spinal cats. J Neurophysiol 79:392–409

    CAS  Google Scholar 

  • Comer CM, Robertson RM (2001) Identified nerve cells and insect behavior. Prog Neurobio 63:409–439

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Cruse H (1976) The function of legs in the free walking stick insect, Carausius morosus. J Comp Physiol A 112:135–162

    Google Scholar 

  • Cruse H (1985) Coactivating influences between neighbouring legs in walking insects. J Exp Biol 114:513–519

    Google Scholar 

  • Cruse H, Schwarze W (1988) Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus). J Exp Biol 138:455–469

    Google Scholar 

  • Dasari S, Cooper RL (2004) Modulation of sensoryCNSmotor circuits by serotonin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Delcomyn F (1971) Locomotion of the cockroach Periplaneta americana. J Exp Biol 54:443–452

    Google Scholar 

  • Drew T (1988) Motor cortical cell discharge during voluntary gait modification. Brain Res 457:181–187

    Article  CAS  PubMed  Google Scholar 

  • Drew T (1993) Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. J Neurophysiol 70:179–199

    CAS  PubMed  Google Scholar 

  • Drew T, Prentice S, Schepens B (2004) Cortical and brainstem control of locomotion. Prog Brain Res 143:251–261

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Full RJ, Tu MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156:215–231

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Grillner S (1997) Ion channels and locomotion. Science 278:1087–1088

    Article  CAS  PubMed  Google Scholar 

  • Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573–586

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jindrich DL, Full RJ (1999) Many-legged maneuverability: dynamics of turning in hexapods. J Exp Biol 202:1603–1623

    PubMed  Google Scholar 

  • Johnston RM, Levine RB (1996) Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. J Neurophysiol 76:3178–3195

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Kiehn O, Eken T (1997) Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? J Neurophysiol 78:3061–3068

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Kien J, Altman J (1992) Preparation and execution of movement: parallels between insects and mammalian motor systems. Comp Biochem Physiol 103A:15–24

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • McLean DL, Sillar KT (2003) Spinal and supraspinal functions of noradrenaline in the frog embryo: consequences for motor behaviour. J Physiol 551:575–587

    Article  CAS  PubMed  Google Scholar 

  • Neter J, Kutner M, Nachtsheim C, Wasserman W (1996) Applied linear statistical models. The McGraw-Hill Companies Inc., Boston MA

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pearson K, Fourtner C (1975) Nonspiking interneurons in the walking system of the cockroach. J Neurophysiol 38:33–52

    CAS  PubMed  Google Scholar 

  • Pearson K, Iles J (1970) Discharge patters of the coxal levators and depressor motorneurons of the cockroach. J Exp Biol 52:139–165

    CAS  PubMed  Google Scholar 

  • Pombal MA, Marin O, Gonzalez A (2001) Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain. J Comp Neurol 431:105–126

    Article  CAS  PubMed  Google Scholar 

  • Quinlan KA, Placas PG, Buchanan JT (2004) Cholinergic modulation of the locomotor network in the lamprey spinal cord. J Neurophysiol 92:1536–1548

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Roeder K (1937) The control of tonus and locomotor activity in the praying mantis (Mantis religiosa L.). J Exp Biol 76:353–374

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ryckebusch S, Laurent G (1993) Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. J Neurophysiol 69:1583–1595

    CAS  PubMed  Google Scholar 

  • Schaefer P, Ritzmann R (2001) Descending influences on escape behavior and motor pattern in the cockroach. J Neurobio 49:9–28

    Article  CAS  Google Scholar 

  • Selverston A (1999) What invertebrate circuits have taught us about the brain. Brain Res Bull 50:439–440

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Wang H, Jung R (2002) Variability analyses that supraspino-spinal interactions provide dynamic stability in motor control. Brain Res 930:83–100

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wilson DM (1966) Insect walking. Ann Rev Entomol 11:103–122

    Article  CAS  Google Scholar 

  • Zhang W, Grillner S (2000) The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey. Brain Res 879:188–192

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

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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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  1. Department of Biology, Case Western Reserve University, 10900 Euclid Ave., Cleveland, OH, 44106-7080, USA

    Angela L. Ridgel & Roy E. Ritzmann

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  1. Angela L. Ridgel
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  2. Roy E. Ritzmann
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Correspondence to Angela L. Ridgel.

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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

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