Instantaneous kinematic phase reflects neuromechanical response to lateral perturbations of running cockroaches

Biological Cybernetics

Volumn 107, Issue 2, 2013, Pages 179-200

  Revzen, Shai ^a   Burden, Samuel A ^b   Moore, Talia Y ^a   Mongeau, Jean Michel ^a   Full, Robert J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomechanics; Cockroach; Locomotion; Neural clock; Neuromechanical control; Perturbation; Phase

Indexed keywords

CENTRAL PATTERN GENERATOR; COCKROACH; INSTANTANEOUS KINEMATICS; NEURAL OSCILLATOR; PERTURBATION; PHASE; RHYTHMIC MOVEMENTS; TRADITIONAL APPROACHES;

ANIMALS; BIOMECHANICS; BIPED LOCOMOTION; RECOVERY;

KINEMATICS;

ANIMALIA; BLABERUS DISCOIDALIS; BLATTARIA; HEXAPODA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; BODY EQUILIBRIUM; COCKROACH; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; FEEDBACK SYSTEM; HEMISPHERIC DOMINANCE; NONLINEAR SYSTEM; PERIODICITY; PHYSIOLOGY; RUNNING; SKELETAL MUSCLE; VIDEORECORDING;

ANIMALS; BIOMECHANICS; COCKROACHES; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEEDBACK, PHYSIOLOGICAL; FUNCTIONAL LATERALITY; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; NONLINEAR DYNAMICS; PERIODICITY; POSTURAL BALANCE; RUNNING; VIDEO RECORDING;

EID: 84876289974     PISSN: 03401200     EISSN: 14320770     Source Type: Journal    
DOI: 10.1007/s00422-012-0545-z     Document Type: Article

References (95)

1. Ahn AN, Full RJ (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(3):379-389
2. Ahn AN, Meijer K, Full RJ (2006) In situ muscle power differs without varying in vitro mechanical properties in two insect leg muscles innervated by the same motor neuron. J Exp Biol 209(17), 3370-3382. ISSN 0022-0949. doi: 10.1242/jeb.02392
3. Altendorfer R, Koditschek DE, Holmes P (2004) Stability analysis of legged locomotion models by symmetry-factored return maps. Int J Rob Res. 23(10-11):979-999
4. Altendorfer R, Moore N, Komsuolu H, Buehler M, Brown HB, McMordie D, Saranli U, Full RJ, Koditschek DE (2001) Rhex: a biologically inspired hexapod runner. Auton Rob 11(3):207-213. ISSN 1573-7527. doi: 10.1023/A:1012426720699
5. Bachmann RJ, Boria FJ, Vaidyanathan R, Ifju PG, Quinn RD (2009) A biologically inspired micro-vehicle capable of aerial and terrestrial locomotion. Mech Mach Theory 44(3):513-526. ISSN 0094-114X doi: 10.1016/j.mechmachtheory.2008.08.008
6. Bender JA, Pollack AJ, Ritzmann RE (2010) Neural activity in the central complex of the insect brain is linked to locomotor changes. Curr Biol 20:921-926
7. Büschges A (2005) Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. J Neurophysiol 93:1127-1135. doi: 10.1152/jn.00615.2004
8. Büschges A, Scholz H, El-Manira A (2011) New moves in motor control. Curr Biol 21:R513-R524. doi: 10.1016/j.cub.2011.05.029
9. Carbonell C (1947) The thoracic muscles of the cockroach Periplaneta americana (L.). Smith Misc Coll 107:1-23
10. Cruse H, Knauth A (1989) Coupling mechanisms between the contralateral legs of a walking insect (Carausius morosus). J Exp Biol 144:199-213
11. Cruse H, Schwarze W (1988) Mechanisms of coupling between the ipsilateral legs of a walking insect (Carausius morosus). J Exp Biol 138:455-469
12. Cruse H, Durr V, Schmitz J (2007) Insect walking is based on a decentralized architecture revealing a simple and robust controller. Philos Trans R Soc A 365(1850):221-250
13. Cruse H, Kinderman T, Schumm M, Dean J, Schmitz J (1998) Walknet - a biologically inspired network to control six-legged walking. Neural Netw. 11(7-8):1435-1447
14. Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210(4469):492-498. doi: 10.1126/science.7423199
15. Dudek DM, Full RJ (2007) An isolated insect leg's passive recovery from dorso-ventral perturbations. J Exp Biol 210:3209-3217. doi: 10.1242/jeb.008367
16. Duysens J, Clarac, Cruse H (2000) Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80(1):83-133. ISSN 0031-9333. http://physrev.physiology.org/cgi/content/abstract/80/1/83
17. Fisher NI (1993) Statistical analysis of circular data. Cambridge University Press, Cambridge. ISBN 0-521-35018-2
18. Floquet G (1883) Sur les Equations différentielles linéaires à coefficients périodiques. Ann Sci Ecole Norm Sup 2:12
19. Fuchs E, Holmes P, Kiemel T, Ayali A (2011) Intersegmental coordination of cockroach locomotion: adaptive control of centrally coupled pattern generator circuits. Front Neural Circuits 4. doi: 10.3389/fncir.2010.00125
20. Fuchs E, Holmes P, David I, Ayali A (2012) Proprioceptive feedback reinforces centrally generated stepping patterns in the cockroach. J Exp Biol 215:1884-1891. doi: 10.1242/jeb.067488
21. Full RJ, Tu MS (1990) Mechanics of 6-legged runners. J Exp Biol 148:129-146. ISSN 0022-0949
22. Full RJ, Blickhan R, Ting LH (1991) Leg design in hexapedal runners. J Exp Biol 158:369-390. ISSN 0022-0949
23. Full RJ, Stokes DR, Ahn A, Josephson RK (1998) Energy absorption during running by leg muscles in a cockroach. J Exp Biol 201: 997-1012
24. Full RJ, Koditschek DE (1999) Templates and anchors: neuromechanical hypotheses of legged locomotion on land. J Exp Biol 202: 3325-3332
25. Ghigliazza RM, Altendorfer R, Holmes P, Koditschek DE (2005) A simply stabilized running model. SIAM Rev 47(3):519-549
26. Grillner S (1972) The role of muscle stiffness in meeting the changing postural and locomotor requirements for force development by the ankle extensors. Acta Physiol Scand 86:92-108
27. Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228:143-149
28. Grillner S, Wallén P (2002) Cellular bases of a vertebrate locomotor system - steering, intersegmental and segmental co-ordination and sensory control. Brain Res Rev 40(1-3):92-106
29. Guckenheimer J, Holmes P (1983) Nonlinear oscillations, dynamical systems, and bifurcations of vector fields. Springer, Berlin
30. Holmes P, Full RJ, Koditschek D, Guckenheimer J (2006) Dynamics of legged locomotion: models, analyses, and challenges. SIAM Rev 48(2):207-304
31. Holtje M, Hustert R (2003) Rapid mechano-sensory pathways code leg impact and elicit very rapid reflexes in insects. J Exp Biol 206(16):2715-2724. ISSN 0022-0949. doi: 10.1242/jeb.00492
32. Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw. 21(4):642-653. ISSN 0893-6080. doi: 10.1016/j.neunet.2008.03.014
33. Jaric S, Latash ML (2000) The equilibrium-point hypothesis is still doing fine. Hum Mov Sci 19(6):933-938
34. Jindrich DL, Full RJ (1999) Many-legged maneuverability: dynamics of turning in hexapods. J Exp Biol 202(12):1603-1623
35. Jindrich DL, Full RJ (2002) Dynamic stabilization of rapid hexapedal locomotion. J Exp Biol 205(18):2803-2823. ISSN 0022-0949
36. Kalman RE (1960) A new approach to linear filtering and prediction problems. J Basic Eng 82:35-45
37. Kim S, Clark JE, Cutkosky MR (2006) iSprawl: design and tuning for high-speed autonomous open-loop running. Int J Robot Res 25(9):903-912. ISSN 0278-3649. doi: 10.1177/0278364906069150
38. Klavins E, Komsuoglu H, Full RJ, Koditschek DE (2002) The role of reflexes versus central pattern generators in dynamical legged locomotion. In: Ayers J, Davis J, Rudolph A (eds) Neurotechnology for biomimetic robots. MIT Press, Cambridge, pp 351-382
39. Kralemann B, Cimponerlu L, Rosenblum M, Pikovsky A, Mrowka R (2007) Uncovering interaction of coupled oscillators from data. Phys Rev E 76(5):055201. ISSN: 1539-3655. doi: 10.1103/PhysRevE.76.055201
40. Kram R, Wong B, Full RJ (1997) Three-dimensional kinematics and limb kinetic energy of running cockroaches. J Exp Biol 200(13):1919-1929. ISSN 0022-0949
41. Kubow TM, Full RJ (1999) The role of the mechanical system in control: a hypothesis of self-stabilization in hexapedal runners. Phil Trans R Soc B 354(1385):849-861. ISSN 0962-8436
42. Kukillaya RP, Holmes PJ (2007) A hexapedal jointed-leg model for insect locomotion in the horizontal plane. Biol Cybern 97(5-6): 379-395. ISSN 0340-1200. doi: 10.1007/s00422-007-0180-2
43. Kukillaya RP, Holmes P (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. doi: 10.1016/j.jtbi.2009.07.036
44. Kukillaya R, Proctor J, Holmes P (2009) Neuromechanical models for insect locomotion: stability, maneuverability, and proprioceptive feedback. Chaos 19(2). ISSN 1054-1500. doi: 10.1063/1.3141306
45. MacKay-Lyons M (2002) Central pattern generation of locomotion: a review of the evidence. Phys Ther 82(1):69-83. ISSN 0031-9023. http://www.ptjournal. org/cgi/content/abstract/82/1/69
46. Maes LD, Herbin M, Hackert R, Bels VL, Abourachid A (2008) Steady locomotion in dogs: temporal and associated spatial coordination patterns and the effect of speed. J Exp Biol 211:138-149. doi: 10.1242/jeb.008243
47. Marder E, Bucher D, Schulz D, Taylor A (2005) Invertebrate central pattern generator moves along. Curr Biol 15:685-699
48. Mazo M, Tabuada P (2009) Input-to-state stability of self-triggered control systems. In: Conference on decision and control, 48th IEEE, pp 928-933
49. Noah JA, Quimby L, Frazier SF, Zill SN (2004) Walking on a peg leg: extensor muscle activities and sensory feedback after distal leg denervation in cockroaches. J Comp Physiol A 190:217-231. ISSN 0340-7594. doi: 10.1007/s00359-003-0488-x
50. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Ann Rev Neurosci 16:265-297
51. Pearson KG (1995) Proprioceptive regulation of locomotion. Curr Opin Neurobiol 5:786-791
52. Pearson KG (2004) Generating the walking gait: role of sensory feedback. Prog Brain Res 143:123-129
53. Pearson KG, Iles JF (1971) Innervation of coxal depressor muscles in cockroach, Periplaneta americana. J Exp Biol 54(1):215-232
54. Pearson KG, Collins DF (1993) Reversal of the influence of group Ib afferents from plantaris on activity in medial gastrocnemius-muscle during locomotor-activity. J Neurophysiol 70(3):1009-1017. ISSN 0022-3077
55. Politis DN (1995) A primer on bootstrap methods in statistics. Technical report 95-19. Purdue University. http://www.stat.purdue.edu/research/technical- reports/pdfs/1995/tr95-19.pdf
56. Politis DN (1998) Computer-intensive methods in statistical analysis. IEEE Signal Proc Mag 15(1):39-55. ISSN 1053-5888. doi: 10.1109/79.647042
57. Prochazka A, Gillard D, Bennett DJ (1997a) Implications of positive feedback in the control of movement. J Neurophysiol 77(6):3237-3251. ISSN 0022-3077
58. Prochazka A, Gillard, D, Bennett DJ (1997b) Positive force feedback control of muscles. J Neurophysiol 77(6):3226-3236. ISSN 0022-3077
59. Proctor J, Holmes PJ (2008) Steering by transient destabilization in piecewise-holonomic models of legged locomotion. Regul Chaotic Dyn 13(4):267-282. doi: 10.1134/S1560354708040047
60. Proctor J, Holmes PJ (2010) Reflexes and preflexes: on the role of sensory feedback on rhythmic patterns in insect locomotion. Biol Cybern 102:513-531. doi: 10.1007/s00422-010-0383-9
61. Proctor J, Kukillaya RP, Holmes P (2010) A phase-reduced neuro-mechanical model for insect locomotion: feed-forward stability and proprioceptive feedback. Phil Trans R Soc A 368:5087-5104
62. Pullin AO, Kohut NJ, Zarrouk D, Fearing RS (2012) Dynamic turning of 13 cm robot comparing tail and differential drive. In: IEEE international conference on robotics and automation, May
63. Quinn RD, Ritzmann RE (1998) Construction of a hexapod robot with cockroach kinematics benefits both robotics and biology. Connect Sci 10(3-4):239-254. ISSN 0954-0091. doi: 10.1080/095400998116422
64. Rauch HE, Tung F, Striebel CT (1965) Maximum likelihood estimates of linear dynamic systems. AIAA J 3(8):1445-1450. ISSN 0001-1452
65. Revzen S (2009) Neuromechanical control architectures of arthropod locomotion. PhD Thesis. University of California, Berkeley
66. Revzen S, Guckenheimer JM (2008) Estimating the phase of synchronized oscillators. Phys Rev E 78(5):051907. ISSN 1539-3755. doi: 10.1103/PhysRevE.78. 051907
67. Revzen S, Koditschek DE, Full RJ (2008) Towards testable neuromechanical control architectures for running. In: Sternad D (ed) Progress in motor control - a multidisciplinary perspective, pp 25-56. Springer, New York doi: 10.1007/978-0-387-77064-2-3
68. Ridgel AL, Ritzmann RE (2005) Effects of neck and circumoesophageal connective lesions on posture and locomotion in the cockroach. J Comp Physiol A 191(6):559-573
69. Ridgel A, Frazier F, Zill SN (2001) Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches. J Comp Physiol A 187(5):405-420. doi: 10.1007/s003590100213
70. Ritzmann RE, Büschges A (2007) Adaptive motor behavior in insects. Curr Opin Neurobiol 17(6):629-636. ISSN 0959-4388. doi: 10.1016/j.conb.2008.01. 001
71. Schilling M, Cruse H, Arena P (2007) Hexapod walking: an expansion to walknet dealing with leg amputations and force oscillations. Biol Cybern 96(3):323-340. ISSN 0340-1200. doi: 10.1007/s00422-006-0117-1
72. Schmitt J, Holmes P (2000a) Mechanical models for insect locomotion: dynamics and stability in the horizontal plane I. Theory. Biol Cybern 83(6):501-515
73. Schmitt J, Holmes P (2000b) Mechanical models for insect locomotion: dynamics and stability in the horizontal plane II. Application. Biol Cybern 83(6):517-527
74. Schmitt J, Holmes P (2001) Mechanical models for insect locomotion: stability and parameter studies. Physica D 156(1-2):139-168
75. Schmitt J, Holmes P (2003) Mechanical models for insect locomotion: active muscles and energy losses. Biol Cybern 89(1): 43-55. ISSN 0340-1200. doi: 10.1007/s00422-003-0404-z
76. Schmitt J, Garcia M, Razo RC, Holmes P, Full RJ (2002) Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects. Biol Cybern 86(5):343-353
77. Seyfarth A, Geyer H, Herr H (2003) Swing-leg retraction: a simple control model for stable running. J Exp Biol 206(15):2547-2555
78. Spagna JC, Goldman DI, Lin P-C, Koditschek DE, Full RJ (2007) Distributed mechanical feedback in arthropods and robots simplifies control of rapid running on challenging terrain. Bioinspir Biomim 2(1): 9-18. ISSN 1748-3182. doi: 10.1088/1748-3182/2/1/002
79. Spenko MJ, Haynes GC, Saunders JA, Cutkosky MR, Rizzi AA, Full RJ, Koditschek DE (2008) Biologically inspired climbing with a hexapedal robot. J Field Robot 25(4-5):223-242. ISSN 1556-4959. doi: 10.1002/rob.20238
80. Spence AJ, Revzen S, Seipel J, Mullens C, Full RJ (2010) Insects running on elastic surfaces. J Exp Biol 213:1907-1920. ISSN 0022-0949. doi: 10.1242/jeb.042515
81. Sponberg S, Full RJ (2008) Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain. J Exp Biol 211(3):433-446. ISSN 0022-0949. doi: 10.1242/jeb.012385
82. Sponberg S, Libby T, Mullens C, Full RJ (2011a) Shifts in a single muscle's control potential of body dynamics. Phil Trans R Soc B 366:1606-1620. doi: 10.1098/rstb.2010.0368
83. Sponberg S, Spence A, Mullens C, Full RJ (2011b) A single muscle's multifunctional control potential of body dynamics for postural control and running. Philos Trans R Soc B 366:1592-1605. doi: 10.1098/rstb.2010.0367
84. Tabuada P (2007) Event-triggered real-time scheduling of stabilizing control tasks. IEEE Trans Autom Control 52(9):1680-1685. ISSN 0018-9286. doi: 10.1109/TAC.2007.904277
85. Ting LH, Blickhan R, Full RJ (1994) Dynamic and static stability in hexapedal runners. J Exp Biol 197:251-269. ISSN 0022-0949
86. Watson JT, Ritzmann RE (1998a) Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: I. Slow running. J Comp Physiol A 182(1):11-22. ISSN 0340-7594. doi: 10.1007/s003590050153
87. Watson JT, Ritzmann RE (1998b) Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis: II. Fast running. J Comp Physiol A 182(1):23-33. ISSN 0340-7594. doi: 10.1007/s003590050154
88. Watson JT, Ritzmann RE, Pollack AJ (2002a) Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement. J Comp Physiol A 188(1):55-69. ISSN 0340-7594. doi: 10.1007/s00359-002-0278-x
89. Watson JT, Ritzmann RE, Zill SN, Pollack AJ (2002b) Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics. J Comp Physiol A 188(1):39-53. ISSN 0340-7594. doi: 10.1007/s00359-002-0277-y
90. Webb B (2002) Robots in invertebrate neuroscience. Nature 417(6886):359-363. ISSN 0028-0836
91. Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471-490
92. Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58(2):185-205. ISSN 0301-0082
93. Zill SN, Moran DT, Varela, FG (1981) The exoskeleton and insect proprioception. 2. Reflex effects of tibial campaniform sensilla in the american cockroach, Periplaneta americana. J Exp Biol 94:43-55. ISSN 0022-0949
94. Zill SN, Schmitz J, Büschges A (2004) Load sensing and control of posture and locomotion. Arthropod Struct Dev 33(3):273-286. ISSN 1467-8039. doi: 10.1016/j.asd.2004.05.005
95. Zill SN Keller BR, Duke ER (2009) Sensory signals of unloading in one leg follow stance onset in another leg: transfer of load and emergent coordination in cockroach walking. J Neurophysiol 101(5):2297-2304. ISSN 0022-3077. doi: 10.1152/jn.00056.2009