Pattern generation for stick insect walking movements - Multisensory control of a locomotor program

Brain Research Reviews

Volumn 27, Issue 1, 1998, Pages 65-88

  Bässler, Ulrich ^a   Büschges, Ansgar ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Pattern generation; Stick insect; Walking

Indexed keywords

INSECT; LEG MOVEMENT; LOCOMOTION; NERVE CELL NETWORK; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; REVIEW; SENSE ORGAN; WALKING;

EID: 0032102058     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(98)00006-X     Document Type: Article

References (124)

1. [1] D. Bässler, A. Büschges, S. Meditz, U. Bässler, Correlation between muscle structure and filter characteristics of the muscle-joint system in three orthopteran insect species, J. Exp. Biol. 199 (1996) 2169-2183.
2. [2] U. Bässler, Zur Regelung der Stellung des Femur-Tibia-Gelenkes bei der Stabheuschrecke Carausius morosus in der Ruhe und im Lauf, Kybernetik 4 (1967) 18-26.
3. [3] U. Bässler, Reversal of a reflex to a single motoneuron in the stick insect Cuniculina impigra, Biol. Cybernetics 24 (1976) 47-49.
4. [4] U. Bässler, Sense organs in the femur of the stick insect and their relevance to the control of position of the femur-tibia joint, J. Comp. Physiol. 121 (1977) 99-113.
5. [5] U. Bässler, Neural Basis of Elementary Behavior in Stick Insects, Springer, Berlin, 1983, 166 pp.
6. [6] U. Bässler, On the definition of central pattern generator and its sensory control, Biol. Cybernetics 54 (1986) 65-69.
7. [7] U. Bässler, Timing and shaping influences on the motor output for walking in stick insects, Biol. Cybernetics 55 (1987) 397-401.
8. [8] U. Bässler, Functional principles of pattern generation for walking movements of stick insect forelegs: the role of the femoral chordotonal organ afferences, J. Exp. Biol. 136 (1988) 125-147.
9. [9] U. Bässler, Variability of femoral chordotonal organ reflexes in the locust, Locusta migratoria, Physiol. Entomol. 17 (1992) 208-212.
10. [10] U. Bässler, The walking (and searching) pattern generator of stick insects, a modular system composed of reflex chains and endogenous oscillators, Biol. Cybernetics 69 (1993) 305-317.
11. [11] U. Bässler, The femur-tibia control system of stick insects - a model system for the study of the neural basis of joint control, Brain Res. Rev. 18 (1993) 207-226.
12. [12] U. Bässler, A. Büschges, Interneurones participating in the 'active reaction' in stick insects, Biol. Cybernetics 62 (1990) 529-538.
13. [13] U. Bässler, E. Foth, G. Breutel, The inherent walking direction differs for the prothoracic and metathoracic legs of stick insects, J. Exp. Biol. 116 (1985) 301-311.
14. [14] U. Bässler, U.T. Koch, Modelling of the active reaction of stick insects by a network of neuromimes, Biol. Cybernetics 62 (1989) 141-150.
15. [15] U. Bässler, J. Rohrbacher, G. Karg, G. Breutel, Interruption of searching movements of partly restrained front legs of stick insects, a model situation for the start of a stance phase?, Biol. Cybernetics 65 (1991) 507-514.
16. [16] U. Bässler, W. Stein, Contributions of structure and innervation pattern of the stick insect extensor tibiae muscle to the filter characteristics of the muscle-joint system, J. Exp. Biol. 199 (1996) 2185-2198.
17. [17] U. Bässler, J. Storrer, The neural basis of the femur-tibia control system in the stick insect Carausius morosus: I. Motoneurones of the extensor tibiae muscle, Biol. Cybernetics 38 (1980) 107-114.
18. [18] U. Bässler, U. Wegner, Motor output of the denervated thoracic ventral nerve cord in the stick insect Carausius morosus, J. Exp. Biol. 105 (1983) 127-145.
19. [19] T.G. Brown, Die Reflexfunktionen des Zentralnervensystems mit besonderer Berücksichtigung der rhythmischen Tätigkeiten beim Säugetier, Erg. Physiol. 15 (1916) 480-790.
20. [20] D.E. Brunn, J. Dean, Intersegmental and local interneurons in the metathorax of the stick insect Carausius morosus that monitor middle leg position, J. Neurophys. 72 (1994) 1208-1219.
21. [21] W.v. Buddenbrock, Der Rhythmus der Schreitbewegungen der Stabheuschrecke Dyxippus, Biol. Zentralblatt 41 (1921) 41-48.
22. [22] M. Burrows, Parallel processing of proprioceptive signals by spiking local interneurons and motor neurons in the locust, J. Neurosci. 7 (1987) 1064-1080.
23. [23] M. Burrows, Local circuits for the control of leg movements in an insect, Trends Neurosci. 15 (1992) 226-232.
24. [24] M. Burrows, The Neurobiology of an Insect Brain, Oxford Univ. Press, Oxford, 1996.
25. [25] M. Burrows, G. Laurent, Reflex circuits and the control of movement, in: R. Durbin, C. Miall, G. Mitchison (Eds.), The Computing Neuron, Addison-Wesley, Wokingham, England, 1989, pp. 244-261.
26. [26] A. Büschges, Untersuchungen zur Reflexaktivierung von Motoneuronen im Regelkreis des Subcoxalgelenkes der indischen Stabheuschrecke Carausius morosus, Diploma Thesis, University of Bielefeld, 1986.
27. [27] A. Büschges, Processing of sensory input from the femoral chordotonal organ by spiking interneurons of stick insects, J. Exp. Biol. 144 (1989) 81-111.
28. [28] A. Büschges, Nonspiking pathways in a joint-control loop of the stick insect Carausius morosus, J. Exp. Biol. 151 (1990) 133-160.
29. [29] A. Büschges, The physiology of sensory cells in the ventral scoloparium of the stick insect femoral chordotonal organ, J. Exp. Biol. 189 (1994) 285-292.
30. [30] A. Büschges, Role of local nonspiking interneurons in the generation of rhythmic motor activity in the stick insect, J. Neurobiol. 27 (1995) 488-512.
31. [31] A. Büschges, Plasticity of neuronal networks that control posture and movement of leg joints in insects, Verh. Dt. Zool. Ges. 88 (1995) 139-151.
32. [32] A. Büschges, C. Böhme, Generation and induction of 'fictive phase transitions' in rhythmic preparations of the stick insect thoracic nerve cord, Proceedings of the 22nd Göttingen Neurobiology Conference, Vol. II, 1994, p. 308.
33. [33] A. Büschges, R. Kittmann, J. Schmitz, Identified nonspiking interneurons in leg reflexes and during walking in the stick insect, J. Comp. Physiol. A 174 (1994) 685-700.
34. [34] A. Büschges, J. Schmitz, U. Bässler, Rhythmic patterns in the thoracic nerve cord of lhe stick insect induced by pilocarpine, J. Exp. Biol. 198 (1995) 435-456.
35. [35] A. Büschges, H. Wolf, Nonspiking local interneurons in insect leg motor control: I. Common layout and species-specific response properties of femur-tibia joint control pathways in stick insect and locust, J. Neurophysiol. 73 (1995) 1843-1860.
36. [36] A. Chrachri, F. Clarac, Induction of rhythmic activity in motoneurones of crayfish thoracic ganglia by cholinergic agonists, Neurosci. Lett. 77 (1987) 49-54.
37. [37] A. Chrachri, F. Clarac, Fictive locomotion in the fourth thoracic ganglion of lhe crayfish, Procambarus clarkii, J. Neurosci. 10 (1990) 707-719.
38. [38] F. Clarac, How do sensory and motor signals interact during locomotion? in: D.R. Humphrey, H.-J. Freund (Eds.), Motor Control: Concept and Issues, Wiley, New York, 1991, pp. 199-221.
39. [39] H. Cruse, The function of the legs in the free walking stick insect, Carausius morosus, J. Comp. Physiol. 112 (1976) 235-262.
40. [40] H. Cruse, The conlrol of the anterior extreme position of the hindleg of a walking insect, Physiol. Entomol. 4 (1979) 121-124.
41. [41] H. Cruse, A quantitative model of walking incorporating central and peripheral influences: II. The connections between the different legs, Biol. Cybernetics 37 (1980) 137-144.
42. [42] H. Cruse, Which parameters control the leg movement of a walking leg? II. The start of swing phase, J. Exp. Biol. 116 (1985) 357-362.
43. [43] H. Cruse, What mechanisms coordinate leg movement in walking arthropods?, Trends Neurosci. 13 (1990) 15-21.
44. [44] H. Cruse, Ch. Bartling, G. Cymbalyuk, J. Dean, M. Dreifert, A modular artificial neural net for controlling a six-legged walking system, Biol. Cybernetics 72 (1995) 421-430.
45. [45] H. Cruse, J. Dean, M. Suilmann, The contributions of diverse sense organs to the control of leg movement by a walking insect, J. Comp. Physiol. A 154 (1984) 695-705.
46. [46] H. Cruse, U. Müller-Wilm, J. Dean, Artificial neuronal nets for a 6-legged walking system, in: J.A. Meyer, H.L. Roitblat, S.W. Wilson (Eds.), From Animals to Animals 2, MIT Press, Cambridge, MA, 1993, pp. 52-60.
47. [47] H. Cruse, G. Saxler, Oscillations of force in the standing leg of a walking stick insect (Carauius morosus), Biol. Cybernetics 36 (1980) 159-163.
48. [48] H. Cruse, J. Schmitz, U. Braun, A. Schweins, Control of body height in a stick insect walking on a treadwheel, J. Exp. Biol. 181 (1993) 141-155.
49. [49] J. Dean, Control of leg protraction in the stick insect: a targeted movement showing compensation for externally applied forces, J. Comp. Physiol. A 155 (1984) 771-781.
50. [50] J. Dean, J. Schmitz, Two groups of sensilla in the ventral coxal hairplate of Carausius morosus have different roles during walking, Physiol. Entomol. 17 (1992) 331-341.
51. [51] J. Dean, G. Wendler, Stick insect locomotion on a walking wheel: interleg coordination of leg position, J. Exp. Biol. 103 (1983) 75-94.
52. [52] B. Debrodt, U. Bässler, Recording from visible neurone somata in the desheathed metathoracic ganglion of the phasmid Extatosoma tiaratum, Zool. Jb. Physiol. 93 (1989) 495-500.
53. [53] B. Debrodt, U. Bässler, Responses of flexor motor neurones to stimulation of the femoral chordotonal organ of the phasmid Extatosoma tiaratum, Zool. Jb. Physiol. 94 (1990) 101-119.
54. [54] F. Delcomyn, Neural basis of rhythmic motor acts, Science 210 (1980) 492-498.
55. [55] F. Delcomyn, Activity and directional sensitivity of leg campaniform sensilla in a stick insect, J. Comput. Physiol. A 168 (1991) 113-119.
56. [56] R. DiCaprio, F. Clarac, Reversal of a walking leg reflex elicited by a muscle receptor, J. Exp. Biol. 90 (1981) 197-203.
57. [57] P.S. Dickinson, M. Moulins, Interactions and combinations between different networks in the stomatogastric nervous system, in: R.M. Harris-Warrick, E. Marder, A.I. Selverston, M. Moulins (Eds.), Dynamic Biological Networks, MIT Press, Cambridge, MA, London, UK, 1992, pp. 139-160.
58. [58] V. Dietz, Human neuronal control of automatic functional movemenls: interaction between central and afferent input, Physiol. Rev. 72 (1991) 33-61.
59. [59] R.B. Driesang, A. Büschges, Physiological changes in central neuronal pathways contributing to the generation of a reflex reversal, J. Comp. Physiol. A 179 (1996) 45-57.
60. [60] J. Duysens, M. Triple, G.A. Horstmann, V. Dietz, Gating and reversal of reflexes in ankle muscles during human walking, Exp. Brain Res. 83 (1990) 351-358.
61. [61] A. El Manira, R.A. DiCaprio, D. Cattaert, F. Clarac, Monosynaptic interjoint reflexes and their central modulation during fictive locomotion in crayfish, Eur. J. Neurosci. 3 (1991) 1219-1231.
62. [62] H. Forssberg, S. Grillner, S. Rossignol, Phase-dependent reflex reversal during walking in chronic spinal cats, Brain Res. 85 (1975) 103-107.
63. [63] E. Foth, U. Bässler, Leg movements of stick insects walking with five legs on a treadwheel and with one leg on a motor driven belt: II. Leg coordination when step-frequencies differ from leg to leg, Biol. Cybernetics 51 (1985) 319-324.
64. [64] H. Füller, A. Ernst, Die Ultrastruktur der femoralen Chordotonalorgane von Carausius morosus Br., Zool. Jahrb. Anat. 91 (1973) 574-601.
65. [65] P. Getting, M.S. Dekin, Mechanisms of pattern generation underlying swimming in Tritonia: IV. Gating of central pattern generator, J. Neurophysiol. 53 (1985) 466-480.
66. [66] D.H. Godden, D. Graham, A preparation of the stick insect Carausius morosus for recording intracellularly from identified neurones during walking, Physiol. Entomol. 9 (1984) 275-286.
67. [67] J.P. Gossard, R.M. Brownstone, I. Barajon, H. Hultborn, Transmission in a locomotor-related group Ib pathway from hindlimb extensor muscles in the cat, Exp. Brain Res. 98 (1994) 213-228.
68. [68] J.P. Gossard, J.M. Cabelguen, S. Rossignol, Phase-dependent modulation of primary afferent depolarization in single cutaneous primary afferents evoked by peripheral stimulation during fictive locomotion in the cat, Brain Res. 537 (1990) 14-23.
69. [69] D. Graham, A behavioral analysis of the temporal organisation of walking movements in the 1st instar and adult stick insect (Carausius morosus): I. Cyclic behavior patterns, Biol. Cybernetics 32 (1972) 139-145.
70. [70] D. Graham, The effect of amputation and leg restrained on the free walking coordination of the stick insect Carauius morosus, J. Comp. Physiol. 116 (1977) 91-116.
71. [71] D. Graham, Pattern and control of walking in insects, Adv. Insect Physiol. 18 (1985) 31-140.
72. [72] D. Graham, U. Bässler, Effects of afference sign reversal on motor activity in walking insects (Carausius morosus), J. Exp. Biol. 91 (1981) 179-193.
73. [73] D. Graham, S. Epstein, Behaviour and motor output pattern for an insect walking on a slippery surface, J. Exp. Biol. 118 (1985) 287-296.
74. [74] S. Grillner, Motor control, in: U.B. Brooks (Ed.), Handbook of Physiology, Section 1: The Nervous System, Vol. 2, Williams & Wilkins, Baltimore, 1981, pp. 1179-1236.
75. [75] S. Grillner, R. Dubuc, Control of locomotion in vertebrates: spinal and supraspinal mechanisms, in: S.G. Waxman (Ed.), Functional Recovery in Neurological Disease, Raven Press, New York, 1988, pp. 425-453.
76. [76] R. Haas, O. Dittberner, A. Büschges, A 'semi-intact' single-walking leg preparation for the investigation of interleg reflexes between middle legs of the stick insect, Proceedings of the 24th Göttingen Neurobiology Conference, Vol. II, 1996, p. 103.
77. [77] F.G. Harmon, Neuromimes: action of a reciprocally inhibitory pair, Science 146 (1964) 1323-1325.
78. [78] D. Hess, A. Büschges, Sensorimotor pathways involved in interjoint reflex action of an insect leg, J. Neurophysiol. 33 (1997) 891-913.
79. [79] T. Hofmann, U. Bässler, Anatomy and physiology of trochanteral campaniform sensilla in the stick insect, Cuniculina impigra, Physiol. Entomol. 7 (1982) 413-426.
80. [80] T. Hofmann, U.T. Koch, Acceleration receptors in the femoral chordotonal organ of the stick insect, Cuniculina impigra, J. Exp. Biol. 114 (1985) 225-237.
81. [81] T. Hofmann, U.T. Koch, U. Bässler, Physiology of the femoral chordotonal organ in the stick insect, Cuniculina impigra, J. Exp. Biol. 114 (1985) 207-223.
82. [82] E.v. Holst, Über den Prozess der zentralnervösen Koordination, Pflüg. Arch. 236 (1935) 149-158.
83. [83] R.M. Johnston, R.B. Levine, Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta, J. Neurophysiol. 76 (1996) 3176-3195.
84. [84] G. Karg, G. Breutel, U. Bässler, Sensory influences on the coordination of two leg joints during searching movements of stick insects, Biol. Cybernetics 64 (1991) 329-335.
85. [85] P.S. Katz, W.N. Frost, Intrinsic neuromodulation: altering neuronal circuits from within, TINS 19 (1996) 54-61.
86. [86] R. Kittmann, J. Schmitz, Functional specialization of the scoloparia of the femoral chordotonal organ in stick insects, J. Exp. Biol. 173 (1992) 91-108.
87. [87] A. Lundberg, Half-centres revisited, Regulatory Function of the CNS, Vol. 1, Adv. Physiol. Sci., 1981, pp. 155-167.
88. [88] A.D. McClellan, Movements and motor patterns of the buccal mass of Pleurobranchea during feeding, regurgitation and rejection, J. Exp. Biol. 98 (1982) 195-211.
89. [89] D.W. Morton, H.J. Chiel, Neural architectures for the adaptive behavior, TINS 17 (1994) 413-419.
90. [90] T.G. Nolen, R.R. Hoy, Initiation of behavior by single neurons: the role of behavioral context, Science 226 (1984) 992-994.
91. [91] U. Nothof, U. Bässler, The network producing the 'active reaction' of stick insects is a functional element of different pattern generating systems, Biol. Cybernetics 62 (1990) 453-462.
92. [92] K.G. Pearson, Central programming and reflex control of walking in the cockroach, J. Exp. Biol. 56 (1972) 173-193.
93. [93] K.G. Pearson, Central pattern generation: a concept under serutiny, Adv. Physiol. Res., Plenum, New York, 1987, pp. 167-185.
94. [94] K.G. Pearson, Common principles of motor control in vertebrates and invertebrates, Annu. Rev. Neurosci. 16 (1993) 265-297.
95. [95] K.G. Pearson, Reflex reversal in the walking system of mammals and arthropods, in: W.R. Ferell, U. Proske (Eds.), Early Control of Movement, Plenum, London, 1995a, pp. 135-141.
96. [96] K.G. Pearson, Proprioceptive regulation of locomotion, Curr. Opin. Neurobiol. 5 (1995) 786-791.
97. [97] K.G. Pearson, D. Collins, Reversal of influence of group Ib afferents from plantaris on activity in medial gastrocnemius during locomotor activity, J. Neurophysiol. 70 (1993) 1009-1017.
98. [98] K.G. Pearson, D. Reye, D.W. Parsons, G. Bicker, Flight-initiating interneuron in the locust, J. Neurophysiol. 53 (1985) 910-925.
99. [99] F. Pfeiffer, H. Cruse, Bionik des Laufens - technische Umsetzung biologischen Wissens, Konstruktion 46 (1994) 261-266.
100. [100] F. Pfeiffer, H.J. Weidemann, J. Eltze, The TM walking machine, in: M. Jamashidi, J. Yuh, Ch. Ngyen, R. Lumia (Eds.), Proceedings of the 5th Int. Symp. on Robotics and Manufacturing, Vol. 2, ASME, New York, 1994, pp. 167-174.
101. [101] H.-J. Pfeiffer, Kontrolle des Flexor-Tibiae Muskels der Gespenstheuschrecke Extatosoma tiaratum in verschiedenen Verhaltenszuständen, Dissertation, Universität Kaiserslautern, 1991.
102. [102] A. Prochazka, Comparison of natural and artificial control of movement, IEEE Trans. Rehab. Eng. 1 (1993) 7-17.
103. [103] R.D. Quinn, K.S. Espenscheid, Control of a hexpod root using biological inpired neuronal network, in: R.D. Beer, R.E. Ritzmann, T. McKenna (Eds.), Biological Neural Networks in Invertebrate Neuroethology and Robotics, Academic Press, New York, 1993, pp. 365-381.
104. [104] G. Radnikow, U. Bässler, Function of a muscle whose apodeme travels through a joint moved by other muscles: why the retractor unguis muscle in stick insects is tripartite and has no antagonist, J. Exp. Biol. 157 (1991) 87-99.
105. [105] S. Rossignol, J.P. Lund, T. Drew, The role of sensory inputs in regulating pattern of rhythmical movements in higher vertebrates, in: A. Cohen, S. Rossignol, S. Grillner (Eds.), Neural Control of Rhythmic Movements in Vertebrates, Wiley, New York, 1988, pp. 210-283.
106. [106] S. Ryckebusch, G. Laurent, Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine, J. Neurophysiol. 69 (1993) 1583-1595.
107. [107] A.E. Sauer, A. Büschges, Flexibility of the neuronal network controlling the femur-tibia joint in the stick insect, Verh. Dtsch. Zool. Ges. 88.1 (1995) 90.
108. [108] A.E. Sauer, A. Büschges, W. Stein, The role of presynaptic afferent inhibition in tuning sensorimotor pathways in an insect joint-control network, J. Neurobiol. 32 (1997) 359-376.
109. [109] A.E. Sauer, R.B. Driesang, A. Büschges, U. Bässler, Information processing in the femur-tibia control loop of stick insects: I. The response characteristics of two nonspiking interneurons result from parallel excitatory and inhibitory inputs, J. Comp. Physiol. A 177 (1995) 145-158.
110. [110] A.E. Sauer, R.B. Driesang, A. Büschges, U. Bässler, Distributed processing on the basis of parallel and antagonistic pathways. Simulation of the femur-tibia control system in the stick insect, J. Comput. Neurosci. 3 (1996) 179-198.
111. [111] J. Schmitz, C. Bartling, D. Brunn, H. Cruse, J. Dean, T. Kindermann, M. Schumm, W. Wagner, Adaptive properties of 'hard-wind' neuronal systems, Verh. Dtsch. Zool. Ges. 88.2 (1995) 165-179.
112. [112] J. Schmitz, A. Büschges, R. Kittmann, Intracellular recordings from nonspiking interneurons in a semi-intact, tethered walking insect, J. Neurobiol. 22 (1991) 907-921.
113. [113] J. Schmitz, G. Hassfeld, The treading-on-tarsus reflex in stick insects: phase dependence and modifications of the motor output during walking, J. Exp. Biol. 143 (1989) 373-388.
114. [114] J. Schmitz, H. Schöwerling, No effects of coxo-trochanteral proprioceptors on extensor tibiae motor neurons in posture control, Proceedings of the 20th Göttingen Neurobiology Conference, 1992, p. 118.
115. [115] P. Skorupski, K. Sillar, Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus leniusculus, J. Neurophysiol. 55 (1986) 689-695.
116. [116] R.B. Stein, C. Capaday, The modulation of human reflexes during functional motor tasks, Trends Neurosci. 11 (1988) 328-332.
117. [117] J.C. Weeks, W.B. Kristan, Initiation, maintenance and modulation of swimming in the medical leech by the activity of a single neurone, J. Exp. Biol. 77 (1978) 71-88.
118. [118] G. Weiland, U.T. Koch, Sensory feedback during active movemenls of stick insects, J. Exp. Biol. 133 (1987) 137-156.
119. [119] G. Wendler, Laufen und Stehen der Stabheuschrecke Carausius morosus: Sinnesborstenfelder in den Beingelenken als Glieder von Regelkreisen, Z. Vergl. Physiol. 48 (1964) 198-250.
120. [120] G. Wendler, The coordination of walking movements in arthropods, Symp. Soc. Exp. Biol. 20 (1966) 229-249.
121. [121] D.M. Wilson, I. Waldron, Model for the generation of the motor output pattern in the flying locust, Proc. Electr. Electron. Eng. 56 (1968) 1058-1064.
122. [122] H. Wolf, Reflex modulation in locusts walking on a treadwheel -intracellular recordings from motor neurons, J. Comp. Physiol. A 170 (1992) 443-462.
123. [123] H. Wolf, A. Büschges, Nonspiking local interneurons in insect leg motor control: II. Role of nonspiking local interneurons in the control of leg swing during walking, J. Neurophysiol. 73 (1995) 1861-1875.
124. [124] S.N. Zill, D.T. Moran, The exoskeleton and insect proprioception: I. Responses of tibial campaniform sensilla to external and muscle generated forces in the American cockroach Periplaneta americana, J. Exp. Biol. 91 (1981) 1-24.