Advertisement

Intersegmental Thoracic Descending Interneurons in the Cockroach Periplaneta americana

  • I. Yu. Severina
  • I. L. Isavnina
  • A. N. Knyazev
Morphological Basics for Evolution of Functions

Abstract

The number, location and morphology of intersegmental descending interneurons, which connect pro- and mesothoracic ganglia with the matathoracic ganglion in the cockroach Periplaneta americana, were investigated herein using a retrograde nickel chloride tracing through one of the connectives that link meso- and metathoracic ganglia. The bodies of stained neurons were aggregated into clusters lying ether ipsilaterally or contralaterally to the axon through which the dye was delivered. Differences in size, architecture and dendrite ramification of ipsi- and contralateral neurons were described. Ipsilateral neurons ramified also ipsilaterally, whereas contralateral neurons formed ramifications on the both sides of the ganglion. The data obtained suggest that adjustment of the walking pattern generator by sensory input from legs is mainly achieved through ipsilateral descending neurons, while adaptation to the environment and brain commands is accomplished through contralateral neurons.

Key words

cockroach prothoracic ganglia mesothoracic ganglia descending neurons 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Delcomyn, F., Walking robots and the central and peripheral control of locomotion in insects, Autonomous Robots, 1999, vol. 7, pp. 259–270.CrossRefGoogle Scholar
  2. 2.
    Ritzmann, R.E., Quinn, R.D., Watson, J.T., and Zill, S.N., Insect walking and biorobotics: a relationship with mutual benefits, BioScience, 2000, vol. 50, pp. 23–33.CrossRefGoogle Scholar
  3. 3.
    Schmitt, J., Garcia, M., Razo, C., Holmes, P., and Full, R.J., Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects, Biol. Cybern., 2002, vol. 86, pp. 343–353.CrossRefGoogle Scholar
  4. 4.
    Holmes, P., Full, R.J., Koditschek, D.E., and Guckenheimer, J., The dynamics of legged locomotion: models, analyses and challenges, SIAM Rev., 2006, vol. 48, pp. 207–304.CrossRefGoogle Scholar
  5. 5.
    Zill, S., Schmitz, J., and Buschges, A., Load sensing and control of posture and locomotion, Arthropod Struct. Dev., 2004, vol. 33, pp. 273–286.CrossRefGoogle Scholar
  6. 6.
    Zill, S.N., Ridgel, A.L., DiCaprio, R.A., and Frazier, S.F., Load signalling by cocroach trochanteral campaniform sensilla, Brain Res., 1999, vol. 822, pp. 271–275.CrossRefGoogle Scholar
  7. 7.
    Noah, J.A., Quimby, L., Frazier, S.F., and Zill, S.N., Sensing the effect of body load in legs: responses of tibial campaniform sensilla to forces applied to the thorax in freely standing cockroaches, J. Comp. Physiol. A, 2004, vol. 190, pp. 201–215.CrossRefGoogle Scholar
  8. 8.
    Kaliyamoorthy, S., Zill, S.N., and Quinn, R.D., Force sensors in hexapod locomotion, Intern. J. Robotics Res., 2005, vol. 24, pp. 563–574.CrossRefGoogle Scholar
  9. 9.
    Gorelkin, V.S., Severina, I.Yu., and Isavnina, I.L., Functional role of leg receptors of the cockroach Periplaneta americana in the system of walking control, J. Evol. Biochem. Physiol., 2013, vol. 49, no. 3, pp. 348–352.CrossRefGoogle Scholar
  10. 10.
    Burrows, M. and Newland, P.L., Correlation between the receptive fields of locust interneurons, their dendritic morphology, and the central projections of mechanosensory neurons, J. Comp. Neurol., 1993, vol. 329 (3), pp. 412–426.CrossRefGoogle Scholar
  11. 11.
    Laurent, G., Thoracic intersegmental interneurones in the locust with mechanoreceptive inputs from a leg, J. Comp. Physiol. A, 1986, vol. 159, pp. 171–186.CrossRefGoogle Scholar
  12. 12.
    Murran, M. and Ritzmann, R.E., Analysis of proprioceptive inputs to DPG interneurons in the cockroach, J. Neurobiol., 1988, vol. 19 (6), pp. 552–570.CrossRefGoogle Scholar
  13. 13.
    Strauss, R. and Heisenberg, M., Coordination of legs during straight walking and turning in Drosophila melanogaster, J. Comp. Physiol. A, 1990, vol. 167 (3), pp. 403–412.CrossRefGoogle Scholar
  14. 14.
    Büschges, A., Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion, J. Neurophysiol., 2005, vol. 93 (3), pp. 1127–1135.CrossRefGoogle Scholar
  15. 15.
    Grabowska, M., Godlewska, E., Schmidt, J., and Daun-Gruhn, S., Quadrupedal gaits in hexapod animals–inter-leg coordination in free-walking adult stick insects, J. Exp. Biol., 2012, vol. 215, pp. 4255–4266.CrossRefGoogle Scholar
  16. 16.
    Ayali, A., Couzin-Fuchs, E., David, I., Gal, O., Holmes, P., and Knebel, D., Sensory feedback in cockroach locomotion: current knowledge and open questions, J. Comp. Physiol. A, 2014, vol. 201 (9), pp. 841–850.CrossRefGoogle Scholar
  17. 17.
    Couzin-Fuchs, E., Kiemel, T., Gal, O., Ayali, A., and Holmes, P., Intersegmental coupling and recovery from perturbations in freely-running cockroaches, J. Exp. Biol., 2015, vol. 218, pp. 285–297.CrossRefGoogle Scholar
  18. 18.
    Borgmann, A., Scharstein, H., and Büschges, A., Intersegmental coordination: influence of a single walking leg on the neighboring segments in the stick insect walking system, J. Neurophysiol., 2007, vol. 98 (3), pp. 1685–1696.CrossRefGoogle Scholar
  19. 19.
    Fuchs, E., Holmes, P., David, I., and Ayali, A., Proprioceptive feedback reinforces centrally generated stepping patterns in the cockroach, J. Exp. Biol., 2012, vol. 215, pp. 1884–1891.CrossRefGoogle Scholar
  20. 20.
    Fuchs, E., Holmes, P., Kiemel, T., and Ayali, A., Inter-segmental coordination of cockroach locomotion: adaptive control of centrally coupled pattern generator circuits, Front. Neural Circ., 2011, vol. 4, p.125.Google Scholar
  21. 21.
    Casagrand, J.L. and Ritzmann, R.E., Localization of ventral giant interneuron connections to VM branch of thoracic interneurons in the cockroach, J. Neurobiol., 1991, vol. 22, pp. 643–658.CrossRefGoogle Scholar
  22. 22.
    Ritzmann, R.E. and Pollack, A.J., Identification of thoracic interneurons that mediate giant interneuron-to-motor pathways in the cockroach, J. Comp. Physiol. A, 1986, vol. 159, pp. 639–654.CrossRefGoogle Scholar
  23. 23.
    Cruse, H., Dean, J., and Suilmann, M., The contributions of diverse sense organs to the control of leg movement by a walking insect, J. Comp. Physiol. A, 1984, vol. 154, pp. 695–705.CrossRefGoogle Scholar
  24. 24.
    Brunn, D.E. and Dean, J., Intersegmental and local interneurons in the metathorax of the stick insect Carausius morosus that monitor middle leg position, J. Neurophysiol., 1994, vol. 72, pp. 1208–1219.CrossRefGoogle Scholar
  25. 25.
    David, I., Holmes, P., and Ayali, A., Endogenous rhythm and pattern-generating circuit interactions in cockroach motor centres, Biol. Open., 2016, vol. 5, pp. 1229–1240.CrossRefGoogle Scholar
  26. 26.
    Camhi, J.M., Escape behavior in the cockroach: distributed neural processing, Experientia, 1988, vol. 44, pp. 401–408.CrossRefGoogle Scholar
  27. 27.
    Camhi, J.M. and Tom, W., The escape behavior of the cockroach Periplaneta americana. I. Turning response to wind puffs, J. Comp. Physiol., 1978, vol. 128, pp. 193–201.CrossRefGoogle Scholar
  28. 28.
    Comer, C.M., Mara, E., Murphy, K.A., Getman, M., and Mungy, M.C., Multisensory control of escape in the cockroach Periplaneta americana. II. Patterns of touch-evoked behavior, J. Comp. Physiol. A, 1994, vol. 174, pp. 13–26.CrossRefGoogle Scholar
  29. 29.
    Schaefer, P.L., Kondagunta, G.V., and Ritzmann, R.E., Motion analysis of escape movements evoked by tactile stimulation in the cockroach, Periplaneta americana, J. Exp. Biol., 1994, vol. 190, pp. 287–294.Google Scholar
  30. 30.
    Westin, J., Langberg, J.J., and Camhi, J.M., Responses of giant interneurons of the cockroach Periplaneta americana to wind puffs of different directions and velocities, J. Comp. Physiol., 1977, vol. 121, pp. 307–324.CrossRefGoogle Scholar
  31. 31.
    Burdohan, J.A. and Comer, C.M., Cellular organization of an antennal mechanosensory pathway in the cockroach, Periplaneta americana, J. Neurosci., 1996, vol. 16, pp. 5830–5843.CrossRefGoogle Scholar
  32. 32.
    Ritzmann, R.E. and Pollack, A.J., Wind activated thoracic interneurons of the cockroach: II. Patterns of connection from ventral giant intemeurons, J. Neurobiol., 1988, vol. 19, pp. 589–611.CrossRefGoogle Scholar
  33. 33.
    Ritzmann, R.E. and Pollack, A.J., Parallel motor pathways from thoracic intemeurons of the ventral giant interneuron system cockroach, Periplaneta americana, J. Neurobiol., 1990, vol. 21, pp. 1219–1235.CrossRefGoogle Scholar
  34. 34.
    Ritzmann, R.E., Pollack, A.J., Hudson, S.E., and Hyvonen, A., Convergence of multi-modal sensory signals at thoracic interneurons of the escape system of the cockroach, Periplaneta americana, Brain Res., 1991, vol. 563, pp. 175–183.CrossRefGoogle Scholar
  35. 35.
    Murrain, M.P. and Ritzmann, R.E., Analysis of proprioceptive inputs to DPG interneurons in the cockroach, J. Neurobiol., 1988, vol. 19, pp. 552–570.CrossRefGoogle Scholar
  36. 36.
    Severina, I.Yu., Isavnina, I.L., and Knyazev, A.N., Topographic anatomy of ascending and descending neurons of the supraesophageal, meso-and metathoracic ganglia in paleo-and neopterous insects, J. Evol. Biochem. Physiol., 2016, vol. 52, no. 5, pp. 397–406.CrossRefGoogle Scholar
  37. 37.
    Knebel, D., Ayali, A., Pflüger, H.-J., and Rillich, J., Rigidity and flexibility: the central basis of inter-leg coordination in the locust, Front. Neural Circuits, 2017, vol. 10, p. 112.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • I. Yu. Severina
    • 1
  • I. L. Isavnina
    • 1
  • A. N. Knyazev
    • 1
  1. 1.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

Personalised recommendations