Reflexes and preflexes: On the role of sensory feedback on rhythmic patterns in insect locomotion

Biological Cybernetics

Volumn 102, Issue 6, 2010, Pages 513-531

  Proctor, J ^a   Holmes, P ^a,b  

^a Princeton University   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Biomechanics; Central pattern generator; Hill muscle model; Legged locomotion; Motoneuron; Neural activation; Phasic feedback; Tonic feedback

Indexed keywords

CENTRAL PATTERN GENERATOR; LEGGED LOCOMOTION; MUSCLE MODELS; NEURAL ACTIVATION; PHASIC FEEDBACK;

ADAPTIVE SYSTEMS; BIOMECHANICS; COMPUTER SIMULATION; MECHANICAL PROPERTIES; NEUROPHYSIOLOGY; SENSORY FEEDBACK; TIME MEASUREMENT;

MUSCLE;

BLATTARIA; HEXAPODA;

ACTION POTENTIAL; ANIMAL; ARTICLE; FEEDBACK SYSTEM; INSECT; LOCOMOTION; MOTONEURON; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; FEEDBACK; INSECTS; LOCOMOTION; MOTOR NEURONS;

EID: 77952010304     PISSN: 03401200     EISSN: 14320770     Source Type: Journal    
DOI: 10.1007/s00422-010-0383-9     Document Type: Article

References (71)

1. AN Ahn RJ Full 2002 A motor and a brake: two leg extensor muscles acting at the same joint manage energy differently in a running insect J Exp Biol 205 379 389 1:STN:280:DC%2BD387ktFGisQ%3D%3D 11854374
2. AN Ahn K Meijer RJ Full 2006 In situ muscle power differs without varying in vitro mechanical properties in two insect leg muscles innvervated by the same motor neuron J Exp Biol 209 3370 3382 10.1242/jeb.02392 1:STN:280:DC%2BD28vpt1OksQ%3D%3D 16916973 (Pubitemid 44534274)
3. T Akay A Büschges 2006 Load signals assist the generation of movement-dependent reflex reversal in the femur-tibia joint of stick insects J Neurophysiol 96 3352 3537
4. T Akay U Bässler P Gerharz A Büschges 2001 The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint J Neurophys 85 2 594 604 1:STN:280:DC%2BD3M3htlyiug%3D%3D
5. T Akay S Haehn J Schmitz A Büschges 2004 Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg J Neurophysiol 92 42 51 10.1152/jn.01271.2003 14999042 (Pubitemid 38802231)
6. A Borgmann SL Hooper A Büschges 2009 Sensory feedback induced by front-leg stepping entrains the activity of central pattern generators in caudal segments of the stick insect walking system J Neurosci 29 9 2972 2983 10.1523/JNEUROSCI.3155-08.2009 1:CAS:528:DC%2BD1MXjt1WlsrY%3D 19261892
7. IE Brown SH Scott GE Loeb 1995 "Preflexes"-programmable, high-gain, zero-delay intrinsic responses of perturbed musculoskeletal systems Soc Neurosci Abstr 21 562.9
8. A Büschges 1998 Inhibitory synaptic drive patterns motoneuronal activity in rhythmic preparations of isolated thoracic ganglia in the stick insect Brain Res 783 262 271 10.1016/S0006-8993(97)01370-X 9507159 (Pubitemid 28131406)
9. A Büschges BC Ludwar D Bucher J Schmidt RA DiCaprio 2004 Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system Eur J Neurosci 12 1856 1862 10.1111/j.1460-9568. 2004.03312.x (Pubitemid 38482573)
10. A Büschges T Akay JP Gabriel J Schmidt 2008 Organizing network action for locomotion: insights from studying insect walking Brain Res Rev 57 162 171 10.1016/j.brainresrev.2007.06.028 17888515 (Pubitemid 350213094)
11. J Connor D Walter R McKown 1977 Neural repetitive firing: modifications of the Hodgkin-Huxley axon suggested by experimental results from crustacean axons Biophys J 18 81 102 10.1016/S0006-3495(77)85598-7 1:CAS:528: DyaE2sXktVehsrk%3D 856318
12. F Delcomyn 1991 Perturbation of the motor system in freely walking cockroaches I. Rear leg amputation and the timing of motor activity in leg muscles J Exp Biol 156 483 502 1:STN:280:DyaK3M3mvVOhtg%3D%3D 2051133
13. F Delcomyn 1991 Perturbation of the motor system in freely walking cockroaches II. The timing of motor activity in leg muscles after amputation of a middle leg J Exp Biol 156 503 517 1:STN:280:DyaK3M3mvVOhtw%3D%3D 2051134
14. Ö Ekeberg 1993 A combined neuronal and mechanical model of fish swimming Biol Cybern 69 363 374
15. Ö Ekeberg S Grillner 1999 Simulations of neuromuscular control in lamprey swimming Phil Trans R Soc B 354 895 902 10.1098/rstb.1999.0441 1:STN:280:DyaK1MzhtFagsA%3D%3D 10382223
16. Ö Ekeberg K Pearson 2005 Computer simulation of stepping in the hind legs of the cat: an examination of mechanisms regulating the stance-to-swing transition J Neurophysiol 94 4256 4268 10.1152/jn.00065.2005 16049149 (Pubitemid 41693764)
17. Ö Ekeberg S Grillner A Landsner 1995 The neural control of fish swimming studied through numerical simulations Adapt Behav 3 363 384 10.1177/105971239500300402
18. Ö Ekeberg M Blumel A Büschges 2004 Dynamic simulation of insect walking Arthropod Struct Dev 33 287 300 10.1016/j.asd.2004.05.002 18089040 (Pubitemid 38969910)
19. AS French RKS Wong 1976 The responses of trochanteral hair plate sensilla in the cockroach to periodic and random displacements Biol Cybern 22 33 38 10.1007/BF00340230
20. Fuchs E (2009) Personal communication. Princeton University, Princeton
21. RJ Full DE Koditschek 1999 Templates and anchors: neuromechanical hypotheses of legged locomotion on land J Exp Biol 202 3325 3332 1:STN:280:DC%2BD3c%2Fjt1Sjsg%3D%3D 10562515
22. JP Gabriel A Büschges 2007 Control of stepping velocity in a single insect leg during walking Philos Trans R Soc Lond A 365 251 271 10.1098/rsta.2006.1912
23. RM Ghigliazza P Holmes 2004 A minimal model of a central pattern generator and motoneurons for insect locomotion SIAM J Appl Dyn Syst 3 4 671 700 10.1137/040607563 (Pubitemid 40578321)
24. RM Ghigliazza P Holmes 2004 Minimal models of bursting neurons: how multiple currents, conductances and timescales affect bifurcation diagrams SIAM J Appl Dyn Syst 3 4 636 670 10.1137/030602307 (Pubitemid 40578320)
25. J Guckenheimer 1975 Isochrons and phaseless sets J Math Biol 1 259 273 10.1007/BF01273747
26. Guckenheimer J, Holmes P (1983) Nonlinear oscillations, dynamical systems, and bifurcations of vector fields. Springer, New York
27. H Hatze 1977 A myocybernetic control model of skeletal muscle Biol Cybern 25 103 119 10.1007/BF00337268 1:STN:280:DyaE2s7ht1Ohug%3D%3D 836914 (Pubitemid 8016598)
28. H Hatze 1978 General myocybernetic control model of skeletal muscle Biol Cybern 28 143 157 10.1007/BF00337136 1:STN:280:DyaE1c7isVehsw%3D%3D 630009 (Pubitemid 8271019)
29. AV Hill 1938 The heat of shortening and the dynamic constants of muscle Proc R Soc Lond B 126 136 195 10.1098/rspb.1938.0050
30. A Hodgkin A Huxley 1952 A quantitative description of membrane current and its application to conduction and excitation in nerve J Physiol 117 500 544 1:STN:280:DyaG3s%2FhsFGjug%3D%3D 12991237
31. P Holmes RJ Full D Koditschek J Guckenheimer 2006 The dynamics of legged locomotion: models, analyses and challenges SIAM Rev 48 2 207 304 10.1137/S0036144504445133 (Pubitemid 43842340)
32. Hoppensteadt FC, Izhikevich EM (1997) Weakly connected neural networks. Springer, New York
33. DL Jindrich RJ Full 2002 Dynamic stabilization of rapid hexapedal locomotion J Exp Biol 205 2803 2823 12177146
34. JH Kotaleski S Grillner A Lansner 1999 Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey I. Segmental oscillations dependent on reciprocal inhibition Biol Cybern 81 317 330 10.1007/s004220050565 1:STN:280:DC%2BD3c%2FgvFWrsA%3D%3D 10541935 (Pubitemid 129553887)
35. JH Kotaleski A Lansner S Grillner 1999 Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey II. Hemisegmental oscillations produced by mutually coupled excitatory neurons Biol Cybern 81 299 315 10.1007/s004220050564 1:STN:280:DC%2BD3c%2FgvFWrsw%3D%3D 10541934
36. RP Kukillaya P Holmes 2007 A hexapedal jointed-leg model for insect locomotion in the horizontal plane Biol Cybern 97 5-6 379 395 10.1007/s00422-007-0180-2 17926063 (Pubitemid 351389122)
37. RP Kukillaya P Holmes 2009 A model for insect locomotion in the horizontal plane: feedforward activation of fast muscles, stability, and robustness J Theor Biol 261 2 210 226 10.1016/j.jtbi.2009.07.036 19660474
38. RP Kukillaya J Proctor P Holmes 2009 Neuro-mechanical models for insect locomotion: stability, maneuverability, and proprioceptive feedback CHAOS: Interdiscip J Nonlinear Sci 19 2 026107 10.1063/1.3141306 1:STN:280: DC%2BD1MvlsFGjug%3D%3D
39. W Lehman AG Szent-Görgyi 1975 Regulation of muscular contraction J Gen Physiol 66 1 30 10.1085/jgp.66.1.1 1:CAS:528:DyaE2MXkslGqsrc%3D 125778
40. GE Loeb IE Brown EJ Cheng 1999 A hierarchical foundation for models of sensorimotor control Exp Brain Res 126 1 1 18 10.1007/s002210050712 1:STN:280:DyaK1M3mtlOqug%3D%3D 10333003 (Pubitemid 29192211)
41. Malkin IG (1949) Methods of Poincaré and Linstedt in the theory of nonlinear oscillations. Gostexisdat, Moscow (in Russian)
42. Malkin IG (1956) Some problems in nonlinear oscillation theory. Gostexisdat, Moscow (in Russian)
43. E Marder 2000 Motor pattern generation Curr Opin Neurobiol 10 6 691 698 10.1016/S0959-4388(00)00157-4 1:CAS:528:DC%2BD3MXkvVehug%3D%3D 11240277 (Pubitemid 32052534)
44. T McMillen TL Williams P Holmes 2008 Nonlinear muscles, passive viscoelasticity and body taper conspire to create neuro-mechanical phase lags in anguilliform swimmers PLoS Comput Biol 4 8 e1000157 10.1371/journal.pcbi. 1000157 1:STN:280:DC%2BD1crotV2itg%3D%3D 18769734
45. JA Noah L Quimby SF Frazier SN Zill 2004 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 190 201 215 10.1007/s00359-003-0487-y 1:STN:280:DC%2BD2c7jsF2ksA%3D%3D (Pubitemid 40876385)
46. KG Pearson 1972 Central programming and reflex control of walking in the cockroach J Exp Biol 56 173 193
47. KG Pearson 1995 Proprioceptive regulation of locomotion Curr Opin Neurobiol 5 786 791 10.1016/0959-4388(95)80107-3 1:CAS:528:DyaK28Xns1alug%3D%3D 8805415 (Pubitemid 26042629)
48. KG Pearson 2000 Motor systems Curr Opin Neurobiol 10 649 654 10.1016/S0959-4388(00)00130-6 1:CAS:528:DC%2BD3cXosVGks70%3D 11084328
49. KG Pearson CR Fourtner 1975 Nonspiking interneurons in walking system of the cockroach J Neurophysiol 38 33 51 1:STN:280:DyaE2M%2FnvVKqsg%3D%3D 162945
50. KG Pearson JF Iles 1970 Discharge patterns of coxal levator and depressor motoneurons of the cockroach, Periplaneta americana J Exp Biol 52 139 165 1:STN:280:DyaE3c7kt1ajsA%3D%3D 5435776
51. KG Pearson JF Iles 1973 Nervous mechanisms underlying intersegmental co-ordination of leg movements during walking in the cockroach J Exp Biol 58 725 744
52. KG Pearson RKS Wong CR Fourtner 1976 Connexions between hair-plate afferents and motoneurones in the cockroach leg J Exp Biol 64 251 266 1:STN:280:DyaE287pt1OqtQ%3D%3D 5571
53. K Pearson Ö Ekeberg A Büschges 2006 Assessing sensory function in locomotor systems using neuro-mechanical simulations Trends Neurosci 29 11 625 631 10.1016/j.tins.2006.08.007 1:CAS:528:DC%2BD28XhtFeqtb7K 16956675 (Pubitemid 44602259)
54. R Rose J Hindmarsh 1989 The assembly of ionic currents in a thalamic neuron I. The three-dimensional model Proc R Soc Lond B 237 267 288 10.1098/rspb.1989.0049 1:STN:280:DyaL1Mzos1Ogsg%3D%3D 2571154 (Pubitemid 19211544)
55. J Schmitt P Holmes 2000 Mechanical models for insect locomotion: dynamics and stability in the horizontal plane-application Biol Cybern 83 6 517 527 10.1007/s004220000180 1:STN:280:DC%2BD3M7jslaiuw%3D%3D 11130584
56. J Schmitt P Holmes 2000 Mechanical models for insect locomotion: dynamics and stability in the horizontal plane-theory Biol Cybern 83 6 501 515 10.1007/s004220000181 1:STN:280:DC%2BD3M7jslaiug%3D%3D 11130583
57. JE Seipel P Holmes RJ Full 2004 Dynamics and stability of insect locomotion: a hexapedal model for horizontal plane motions Biol Cybern 91 2 76 90 10.1007/s00422-004-0498-y 15322851 (Pubitemid 40877301)
58. S Sponberg RJ Full 2008 Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain J Exp Biol 211 433 446 10.1242/jeb.012385 1:STN:280:DC%2BD1c%2Flt12qsg%3D%3D 18203999 (Pubitemid 351347446)
59. AK Tryba RE Ritzmann 2000 Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms J Neurophysiol 83 3323 3336 1:STN:280:DC%2BD3czgslyhsw%3D%3D 10848552
60. AK Tryba RE Ritzmann 2000 Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern J Neurophysiol 83 3337 3350 1:STN:280:DC%2BD3czgslyhsA%3D%3D 10848553
61. JT Watson RE Ritzmann 1998 Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: I. Slow running J Comp Physiol A 182 11 22 10.1007/s003590050153 1:STN:280:DyaK1c7gvFSitA%3D%3D 9447710 (Pubitemid 28104738)
62. JT Watson RE Ritzmann 1998 Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: II. Fast running J Comp Physiol A 182 23 33 10.1007/s003590050154 1:STN:280:DyaK1c7gvFSitQ%3D%3D 9447711 (Pubitemid 28104739)
63. TL Williams G Bowtell NA Curtin 1998 Predicting force generation by lamprey muscle during applied sinusiodal movement using a simple dynamic model J Exp Biol 201 869 875 9464967
64. DM Wilson 1965 Proprioceptive leg reflexes in cockroaches J Exp Biol 43 397 409 1:STN:280:DyaF28%2FpvVyntw%3D%3D 5863752
65. Winfree AT (2001) The geometry of biological time, 2nd edn. Springer, New York
66. RKS Wong KG Pearson 1976 Properties of the trochanteral hair plate and its function in the control of walking in the cockroach J Exp Biol 64 233 249 1:STN:280:DyaE287pt1Oqtw%3D%3D 1270992
67. FE Zajac 1989 Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control CRC Crit Rev Lett Biomed Eng 17 359 411 1:STN:280:DyaK3c%2FgsVeisw%3D%3D
68. SN Zill DT Moran 1981 The exoskeleton and insect proprioception I. Responses of tibial campaniform sensilla to external and muscle-generated force in the American cockroach, Periplaneta americana J Exp Biol 91 1 24
69. SN Zill DT Moran 1981 The exoskeleton and insect proprioception III. Activity of tibial campaniform sensilla during walking in the American cockroach, Periplaneta americana J Exp Biol 94 57 75
70. SN Zill DT Moran FG Varela 1981 The exoskeleton and insect proprioception II. Reflex effects of tibial campaniform sensilla in the American cockroach, Periplaneta americana J Exp Biol 94 43 55
71. SN Zill AL Ridgel RA DiCaprio SF Frazier 1999 Load signalling by cockroach trochanteral campaniform sensilla Brain Res 822 271 275 10.1016/S0006-8993(99)01156-7 1:CAS:528:DyaK1MXhs1OisLo%3D 10082909 (Pubitemid 29222855)