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Intersegmental Thoracic Descending Interneurons in the Cockroach Periplaneta americana

  • Morphological Basics for Evolution of Functions
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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.

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References

  1. Delcomyn, F., Walking robots and the central and peripheral control of locomotion in insects, Autonomous Robots, 1999, vol. 7, pp. 259–270.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Camhi, J.M., Escape behavior in the cockroach: distributed neural processing, Experientia, 1988, vol. 44, pp. 401–408.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    I. Yu. Severina, I. L. Isavnina & A. N. Knyazev

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  1. I. Yu. Severina
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  2. I. L. Isavnina
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  3. A. N. Knyazev
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Correspondence to I. Yu. Severina.

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Original Russian Text © I.Yu. Severina, I.L. Isavnina, A.N. Knyazev, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 6, pp. 421–427.

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Severina, I.Y., Isavnina, I.L. & Knyazev, A.N. Intersegmental Thoracic Descending Interneurons in the Cockroach Periplaneta americana. J Evol Biochem Phys 54, 474–481 (2018). https://doi.org/10.1134/S0022093018060078

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  • DOI: https://doi.org/10.1134/S0022093018060078

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