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

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.

[1]  K. D. Roeder The control of tonus and locomotor activity in the praying mantis (Mantis religiosa L.) , 1937 .

[2]  D. Wilson Insect walking. , 1966, Annual review of entomology.

[3]  K. Pearson,et al.  Discharge patterns of coxal levator and depressor motoneurones of the cockroach, Periplaneta americana. , 1970, The Journal of experimental biology.

[4]  F. Delcomyn The Locomotion of the Cockroach Periplaneta Americana , 1971 .

[5]  Michael H. Kutner Applied Linear Statistical Models , 1974 .

[6]  C. R. Fourtner,et al.  Nonspiking interneurons in walking system of the cockroach. , 1975, Journal of neurophysiology.

[7]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

[8]  J. Altman,et al.  Suboesophageal neurons involved in head movements and feeding in locusts , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  S. Zill,et al.  The Exoskeleton and Insect Proprioception: II. Reflex Effects of Tibial Campaniform Sensilla in the American Cockroach, Periplaneta Americana , 1981 .

[10]  J. Kien The initiation and maintenance of walking in the locust: an alternative to the command concept , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[11]  P. Wallén,et al.  Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. , 1984, The Journal of physiology.

[12]  H. Cruse Coactivating Influences Between Neighbouring Legs in Walking Insects , 1985 .

[13]  R. J. Gregor,et al.  Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat , 1986, Experimental Neurology.

[14]  S. Rossignol,et al.  Recovery of locomotion after chronic spinalization in the adult cat , 1987, Brain Research.

[15]  L. Strong,et al.  Arthropod brain (its evolution, development, structure and functions): A. P. Gupta (Ed.), 588 pp. Published by John Wiley & Sons, New York, 1987. Price £60. ISBN 0-471-82811-4 , 1988 .

[16]  T. Drew,et al.  Motor cortical cell discharge during voluntary gait modification , 1988, Brain Research.

[17]  H. Cruse,et al.  Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus) , 1988 .

[18]  R. Full,et al.  Mechanics of a rapid running insect: two-, four- and six-legged locomotion. , 1991, The Journal of experimental biology.

[19]  J Kien,et al.  Preparation and execution of movement: parallels between insect and mammalian motor systems. , 1992, Comparative biochemistry and physiology. Comparative physiology.

[20]  S. Ryckebusch,et al.  Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. , 1993, Journal of neurophysiology.

[21]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[22]  S. Rossignol,et al.  Noradrenergic agonists and locomotor training affect locomotor recovery after cord transection in adult cats , 1993, Brain Research Bulletin.

[23]  S. Grillner,et al.  Neural networks that co-ordinate locomotion and body orientation in lamprey , 1995, Trends in Neurosciences.

[24]  J. Schmitz,et al.  Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine , 1995, The Journal of experimental biology.

[25]  S. Rossignol,et al.  A comparison of treadmill locomotion in adult cats before and after spinal transection. , 1996, Journal of neurophysiology.

[26]  L. Rowell,et al.  Exercise : regulation and integration of multiple systems , 1996 .

[27]  R. Levine,et al.  Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. , 1996, Journal of neurophysiology.

[28]  S. Rossignol,et al.  Locomotor capacities after complete and partial lesions of the spinal cord. , 1996, Acta neurobiologiae experimentalis.

[29]  O. Kiehn,et al.  Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? , 1997, Journal of neurophysiology.

[30]  J. T. Watson,et al.  Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running , 1997, Journal of Comparative Physiology A.

[31]  M. Gebhardt,et al.  Involvement of the suboesophageal and thoracic ganglia in the control of antennal movements in crickets , 1997, Journal of Comparative Physiology A.

[32]  S. Grillner,et al.  Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis , 1997, The Journal of comparative neurology.

[33]  S Grillner,et al.  Ion Channels and Locomotion , 1997, Science.

[34]  V R Edgerton,et al.  Full weight-bearing hindlimb standing following stand training in the adult spinal cat. , 1998, Journal of neurophysiology.

[35]  V R Edgerton,et al.  Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. , 1998, Journal of neurophysiology.

[36]  G. Bernardi,et al.  The gene-richest bands of human chromosomes replicate at the onset of the S-phase , 1998, Cytogenetic and Genome Research.

[37]  Effects of intrathecal alpha1- and alpha2-noradrenergic agonists and norepinephrine on locomotion in chronic spinal cats. , 1998, Journal of neurophysiology.

[38]  U. Bässler,et al.  Pattern generation for stick insect walking movements—multisensory control of a locomotor program , 1998, Brain Research Reviews.

[39]  S. Rossignol,et al.  Early locomotor training with clonidine in spinal cats. , 1998, Journal of neurophysiology.

[40]  Serge Rossignol,et al.  Effects of Intrathecal α1- and α2-Noradrenergic Agonists and Norepinephrine on Locomotion in Chronic Spinal Cats , 1998 .

[41]  Johnston,et al.  Patterned activation of unpaired median neurons during fictive crawling in manduca sexta larvae , 1999, The Journal of experimental biology.

[42]  Allen Selverston,et al.  What invertebrate circuits have taught us about the brain , 1999, Brain Research Bulletin.

[43]  Full,et al.  Many-legged maneuverability: dynamics of turning in hexapods , 1999, The Journal of experimental biology.

[44]  V R Edgerton,et al.  Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. , 1999, Journal of neurophysiology.

[45]  K. Pearson,et al.  Contribution of sensory feedback to the generation of extensor activity during walking in the decerebrate Cat. , 1999, Journal of neurophysiology.

[46]  A K Tryba,et al.  Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. , 2000, Journal of neurophysiology.

[47]  A K Tryba,et al.  Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern. , 2000, Journal of neurophysiology.

[48]  S. Grillner,et al.  The intrinsic function of a motor system — from ion channels to networks and behavior 1 1 Published on the World Wide Web on 22 November 2000. , 2000, Brain Research.

[49]  S. Grillner,et al.  The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey , 2000, Brain Research.

[50]  O. Marín,et al.  Distribution of choline acetyltransferase‐immunoreactive structures in the lamprey brain , 2001, The Journal of comparative neurology.

[51]  J. Buchanan Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology , 2001, Progress in Neurobiology.

[52]  S. Zill,et al.  Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered , 2001, Journal of Comparative Physiology A.

[53]  U. Bässler,et al.  The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. , 2001, Journal of neurophysiology.

[54]  R. Ritzmann,et al.  Descending influences on escape behavior and motor pattern in the cockroach. , 2001, Journal of neurobiology.

[55]  S. Zill,et al.  Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches , 2001, Journal of Comparative Physiology A.

[56]  Christopher M. Comer,et al.  Identified nerve cells and insect behavior , 2001, Progress in Neurobiology.

[57]  Roy E. Ritzmann,et al.  Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics , 2002, Journal of Comparative Physiology A.

[58]  Anders Lansner,et al.  Mechanisms for lateral turns in lamprey in response to descending unilateral commands: a modeling study , 2002, Biological Cybernetics.

[59]  R. Jung,et al.  Variability analyses suggest that supraspino–spinal interactions provide dynamic stability in motor control , 2002, Brain Research.

[60]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[61]  K. Sillar,et al.  Spinal and supraspinal functions of noradrenaline in the frog embryo: consequences for motor behaviour , 2003, The Journal of physiology.

[62]  C. Comer,et al.  The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions , 2003, Journal of Comparative Physiology A.

[63]  S. Rossignol,et al.  Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats. , 2003, Journal of neurophysiology.

[64]  H. Barbeau,et al.  The effect of noradrenergic drugs on the recovery of walking after spinal cord injury , 2003, Spinal Cord.

[65]  S. Zill,et al.  Walking on a ‘peg leg’: extensor muscle activities and sensory feedback after distal leg denervation in cockroaches , 2004, Journal of Comparative Physiology A.

[66]  U. Bässler,et al.  Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor-driven belt , 1985, Biological Cybernetics.

[67]  T. Drew,et al.  Cortical and brainstem control of locomotion. , 2004, Progress in brain research.

[68]  Roger D. Quinn,et al.  Descending control of body attitude in the cockroach Blaberus discoidalis and its role in incline climbing , 2004, Journal of Comparative Physiology A.

[69]  U. Bässler,et al.  Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor-driven belt , 1985, Biological Cybernetics.

[70]  J. Buchanan,et al.  Cholinergic modulation of the locomotor network in the lamprey spinal cord. , 2004, Journal of neurophysiology.

[71]  R. Cooper,et al.  Modulation of sensory–CNS–motor circuits by serotonin, octopamine, and dopamine in semi-intact Drosophila larva , 2004, Neuroscience Research.

[72]  H. Cruse The function of the legs in the free walking stick insect,Carausius morosus , 1976, Journal of comparative physiology.

[73]  D. Graham Effects of circum-oesophageal lesion on the behaviour of the stick insect Carausius morosus , 1979, Biological Cybernetics.