medigraphic.com
Instituto Nacional de Neurología y Neurocirugía

2019, Number 1

<< Back Next >>

Arch Neurocien 2019; 24 (1)

Neurobiology of insect motor control

Fernández-Villalobos G

Language: Spanish
References: 50
Page: 17-27
PDF size: 1258.39 Kb.


ABSTRACT

What is the neural process that regulates the march? How the nervous system physiology and architecture affect the organism when it´s decide to navigate through the world? For living beings, everything starts with a single step; in this small process, the organisms break the inertia, one of the main forces that bind them to the earth. This first step gives rise to a dance, composed of a series of finely coordinated and orchestrated events in which the animal is able to integrate external and internal elements in order to move in a stable way.
The march of living beings reflects a long evolutionary history, which leads to the construction and adaptation of a series of structures. This review use insects as models, to explain some of the fundamental neuronal elements needed to understand the process of walking. The insects share neural mechanisms of motor control with a large number of organisms, including mammals. We will review those elements that allow insects to coordinate their steps through a series of surfaces and at different speeds without stumbling, trying to explain those processes that have led a series of scientists to follow their steps.


REFERENCES

  1. Jung H, Dasen JS. Evolution of patterning systems and circuit elements for locomotion. Dev Cell 2015;32(4):408–22.

  2. Hennig JA, Golub MD, Lund PJ, Sadtler PT, Oby ER, Quick KM, et al. Constraints on neural redundancy. Elife 2018;7.

  3. Farris SM. Evolution of brain elaboration. Philos Trans R Soc Lond B Biol Sci 2015; 370(1684):20150054.

  4. Dasen JS. Evolution of locomotor rhythms. Trends Neurosci 2018; 41(10):648–51.

  5. Thor S, Thomas JB. Motor neuron specification in worms, flies and mice: conserved and “lost” mechanisms. Curr Opin Genet Dev. 2002;12(5):558–64.

  6. Hrycaj SM, Wellik DM. Hox genes and evolution. F1000Research. 2016;5:859.

  7. Zill SN, Underwood MA, Rowley JC, Moran DT. A somatotopic organization of groups of afferents in insect peripheral nerves. Brain Res. 1980;198(2):253–69.

  8. Ampatzis K, Song J, Ausborn J, El Manira A. Pattern of innervation and recruitment of different classes of motoneurons in adult zebrafish. J Neurosci 2013; 33(26):10875–86.

  9. Niven JE, Graham CM, Burrows M. Diversity and evolution of the insect ventral nerve cord. Annu Rev Entomol 2008; 53(1):253–71.

  10. Chapman RF. The insects structure and function. 5th ed. Cambridge, United Kingdom: Cambridge University Press; 2013; 625-69.

  11. Borgmann A, Büschges A. Insect motor control: methodological advances, descending control and inter-leg coordination on the move. Curr Opin Neurobiol 2015; 33:8–15.

  12. Iriarte-Diaz J. Differential scaling of locomotor performance in small and large terrestrial mammals. J Exp Biol 2002; 2908, 2897-908.

  13. Carhart-Harris RL. The entropic brain-revisited. Neuropharmacol 2018; 142:167–78.

  14. Alexander RM. Energy Requirements for Locomotion. In: Princ Anim Locomot. 1st ed. Princeton,USA: Princeton University Press; 2003:38–52.

  15. Yeldesbay A, Tóth T, Daun S. The role of phase shifts of sensory inputs in walking revealed by means of phase reduction. J Comput Neurosci. 2018;44(3):313–39.

  16. Bender JA, Simpson EM, Tietz BR, et al. Kinematic and behavioral evidence for a distinction between trotting and ambling gaits in the cockroach Blaberus discoidalis. J Exp Biol 2011; 214(12):2057-64.

  17. Cruse H. The function of the legs in the free walking stick insect (Carausius morosus). J Comp Physiol 1976;112(2):235–62.

  18. Hughes GM. the Co-Ordination of insect movements. J Exp Biol. 1952; 29(1887):267–85.

  19. Mendes CS, Bartos I, Akay T, Márka S, Mann RS. Quantification of gait parameters in freely walking wild type and sensory deprived Drosophila melanogaster. Elife 2013; 2.

  20. Revzen S, Burden SA, Moore TY, Mongeau JM, Full RJ. Instantaneous kinematic phase reflects neuromechanical response to lateral perturbations of running cockroaches. Biol Cybern 2013; 107(2):179–200.

  21. Ayali A, Couzin-Fuchs E, David I, Gal O, Holmes P, Knebel D. Sensory feedback in cockroach locomotion: current knowledge and open questions. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2015; 201(9):841-50.

  22. Zill SN, Keller BR, Chaudhry S, Duke ER, Neff D, Quinn R, et al. Detecting substrate engagement: responses of tarsal campaniform sensilla in cockroaches. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2010; 196(6):407–20.

  23. Sherrington CS. Flexion-reflex of the limb, crossed extension-reflex and reflex stepping and standing. J Physiol. 1910; 40(1-2):28-121.

  24. Gray J. Croonian Lecture: Aspects of animal locomotion. Proc R Soc B Biol Sci 1939;128(850):28–62.

  25. Cruse H. What mechanisms coordinate leg movement in walking arthropods? Trends Neurosci 1990; 13(1):15-21.

  26. Proctor JL, Holmes P. The effects of feedback on stability and maneuverability of a phase-reduced model for cockroach locomotion. Biol Cybern 2018; 112(4):387–401.

  27. Cruse H. A quantitative model of walking incorporating central and peripheral influences - I. The control of the individual leg. Biol Cybern 1980; 37(3):131–6.

  28. Marder E, Bucher D. Central pattern generators and the control of rythmic movements. Curr Biol 2001; 11:R986–96.

  29. Gowda SBM, Paranjpe PD, Reddy OV, Thiagarajan D, Palliyil S, Reichert H, et al. GABAergic inhibition of leg motoneurons is required for normal walking behavior in freely moving Drosophila. Proc Natl Acad Sci 2018; 115(9):2115–24.

  30. Zhang HY, Sillar KT. Short-term memory of motor network performance via activity-dependent potentiation of Na +/K + pump function. Curr Biol 2012; 22(6):526–31.

  31. Hess D, Büschges A. Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint. J Neurophysiol 1999; 81(4):1856–65.

  32. Smarandache-Wellmann CR. Arthropod neurons and nervous system. Curr Biol 2016;26(20):R960–5.

  33. Büschges A, Scholz H, El Manira A. New moves in motor control. Curr Biol 2011; 21(13):R513–24.

  34. Büschges A, Schmitz J, Bässler U. Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine. J Exp Biol 1995; 198(2):435–56.

  35. Delcomyn F. The locomotion of the cockroach Periplaneta Americana. J Exp Biol 1971; 54(2):443–52.

  36. Full RJ, Blickhan R, Ting LH. Leg design in hexapedal runners. J Exp Biol 1991; 158:369–90.

  37. Watson JT, Ritzmann RE, Zill SN, Pollack AJ. Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics. J Comp Physiol A 2002; 188(1):39–53.

  38. Mahrous AA, Elbasiouny SM. SK channel inhibition mediates the initiation and amplitude modulation of synchronized burst firing in the spinal cord. J Neurophysiol 2017;118(1):161–75.

  39. Büschges A, Gruhn M. Mechanosensory feedback in walking: from joint control to locomotor patterns. Adv In Insect Phys. 2007;34(07):193–230.

  40. Edwards DH, Prilutsky BI. Sensory feedback in the control of posture and locomotion. Book: Neurobiology of Motor Control 263-304.

  41. Dürr V, Theunissen LM, Dallmann CJ, Hoinville T, Schmitz J. Motor flexibility in insects: adaptive coordination of limbs in locomotion and near-range exploration. Behav Ecol Sociobiol 2018;72(1):15.

  42. Akay T, Bässler U, Gerharz P, Büschges A. The role of sensory signals from the insect Coxa-Trochanteral Joint in Controlling Motor Activity of the Femur-Tibia Joint. J Neurophysiol. 2001; 85(2):594–604.

  43. Duysens J, Clarac F, Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 2000; 80(1):83–133.

  44. Jindrich DL, Full RJ. Dynamic stabilization of rapid hexapedal locomotion. J Exp Biol 2002; 205(18):2803-23.

  45. Luco JV. Increase of synaptic efficacy as a correlate to learning in Blatta orientalis. Physiol Behav 1978; 21(5):743–7.

  46. Luco J V., Aranda LC. An electrical correlate to the process of Learning. Experiments in blatta orientalis. Nature 1964; 201(5019):1330–1.

  47. Luco JV, Aranda LC. Reversibility of an electrical correlate to the process of learning. Nature 1966; 209(5019):205–6.

  48. Strausfeld NJ, Li Y. Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. J Comp Neurol 1999; 409(4):603–25.

  49. Guo P, Ritzmann RE. Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J Exp Biol 2013; 216(6):992–1002.

  50. Knebel D, Rillich J, Nadler L, et al. The functional connectivity between the locust leg pattern generators and the subesophageal ganglion higher motor center. Neurosci Lett 2019; 692, 77–82. https://doi.org/10.1016/j. neulet.2018.10.060




2020     |     www.medigraphic.com