Neuronal control of walking: studies on insects

e-Neuroforum - Tập 6 - Trang 105-112 - 2015
Ansgar Büschges1, Joachim Schmidt1
1Institut für Zoologie, Biozentrum Köln, Universität zu Köln, Cologne, Germany

Tóm tắt

The control of walking in insects is to a substantial amount a function of neuronal networks in the thoracic ganglia. While descending signals from head ganglia provide general commands such as for walking direction and velocity, it is the thoracic central nervous system that controls movements of individual joints and legs. The coordination pattern of legs is velocity dependent. However, a clear stereotypic coordination pattern appears only at high velocities. In accordance with the unit burst oscillator concept, oscillatory networks (central pattern generators (CPGs)) interlocked with movement and load sensors control the timing and amplitude of joint movements. For a leg’s movements different joint CPGs of a leg are mainly coupled by proprioceptors. Differential processing of proprioceptive signals allows a task specific modulation of leg movements, for example, for changing movement direction. A switch between walking and searching movements of a leg is under local control. When stepping into a gap missing sensory input and the activation of a local command neuron evokes stereotypic searching movements of the leg.

Tài liệu tham khảo

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 Bässler U (1988) Functional principles of pattern generation for walking movements of stick insect forelegs: the role of the femoral chordotonal organ afferences. J Exp Biol 136:125–147 Berg E, Büschges A, Schmidt J (2013) Single perturbations cause sustained changes in searching behavior in stick insects. J Exp Biol 216:1064–1074 Berg EM, Hooper SL, Schmidt J, Büschges A (2015) A leg-local neural mechanism mediates the decision to search in stick insect. Curr Biol 25:2012–2017 Berkowitz A, Laurent G (1996) Local control of leg movements and motor patterns during grooming in locusts. J Neurosci 16:8067–8078 Bidaye SS, Machacek C, Wu Y, Dickson BJ (2014) Neuronal control of Drosophila walking direction. Science 344:97–101 Böhm H, Schildberger K (1992) Brain neurons involved in the control of walking in the cricket Gryllus bimaculatus. J Exp Biol 166:113–130 Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, Oxford Büschges A (2005) Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. J Neurophysiol 93:1127–1135 Büschges A, Schmitz J, Bässler U (1995) Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine. J Exp Biol 198:435–456 Büschges A, Ludwar BCh, Bucher D, Schmidt J, DiCaprio RA (2004) Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system. Eur J Neurosci 19:1856–1862 Büschges A, Akay T, Gabriel JP, Schmidt J (2008) Organizing network action for locomotion: insights from studying insect walking. Brain Res Rev 57:162–171 Buschmann T, Ewald A, von Twickel A, Büschges A (2015) Controlling legs for locomotion—insights from robotics and neurobiology. Bioinspir Biomim 10:041001 Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods? Trends Neurosci 13:15–21 Dürr V (2001) Stereotypic leg searching movements in the stick insect: kinematic analysis, behavioural context and simulation. J Exp Biol 204:1589–1604 Elsner N (1974) Neuroethology of sound production in gomphocerine grasshoppers (Orthoptera: acrididae). I. Song patterns and stridulatory movements. J Comp Physiol 88:67–102 Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766 Hägglund M, Dougherty KJ, Borgius L, Itohara S, Iwasato T, Kiehn O (2013) Optogenetic dissection reveals multiple rhythmogenic modules underlying locomotion. Proc Natl Acad Sci 110:11589–11594 Hedwig B, Heinrich R (1997) Identified descending brain neurons control different stridulatory motor patterns in an acridid grasshopper. J Comp Physiol 180:285–294 Hellekes K, Blincow E, Hoffmann J, Büschges A (2012) Control of reflex reversal in stick insect walking: effects of intersegmental signals, changes in direction, and optomotor-induced turning. J Neurophysiol 107:239–249 Knops S, Tóth TI, Guschlbauer C, Gruhn M, Daun-Gruhn S (2013) A neuromechanical model for the neuronal basis of curve walking in the stick insect. J Neurophysiol 109:679–691 Ludwar BC, Westmark S, Büschges A, Schmidt J (2005) Modulation of membrane potential in mesothoracic moto- and interneurons during stick insect front-leg walking. J Neurophysiol 94:2772–2784 Marder E, Calabrese RL (1996) Principles of rhythmic pattern generation. Physiol Rev 76:687–717 Marek PE, Bond JE (2006) Biodiversity hotspots: rediscovery of the world’s leggiest animal. Nature 441:707 Orlovsky G, Deliagina T, Grillner S (1999) Neuronal control of locomotion. Oxford University Press, Oxford Stein PS (2008) Motor pattern deletions and modular organization of turtle spinal cord. Brain Res Rev 57:118–124 Tóth TI, Knops S, Daun-Gruhn S (2012) A neuro-mechanical model explaining forward and backward stepping in the stick insect. J Neurophysiol 107:3267–3280 Wendler G (1965) The co-ordination of walking movements in arthropods. Symp Soc Exp Biol 20:229–249 Westmark S, Oliveira EE, Schmidt J (2009) Pharmacological analysis of tonic activity in motoneurons during stick insect walking. J Neurophysiol 102:1049–1061 Wosnitza A, Bockemühl T, Dübbert M, Scholz H, Büschges A (2013) Inter-leg coordination on the control of walking speed in Drosophila. J Exp Biol 216:480–491 Zill SN, Schmitz J, Chaudhry S, Büschges A (2012) Force encoding in stick insect legs delineates a reference frame for motor control. J Neurophysiol 108:1453–1472 Zill SN, Chaudhry S, Exter A, Büschges A, Schmitz J (2014) Positive force feedback in development of substrate grip in the stick insect tarsus. Arthropod Struct Dev 43:441–455