Journal of Comparative Physiology A

, Volume 201, Issue 9, pp 841–850 | Cite as

Sensory feedback in cockroach locomotion: current knowledge and open questions

  • A. Ayali
  • E. Couzin-Fuchs
  • I. David
  • O. Gal
  • P. Holmes
  • D. Knebel
Review

Abstract

The American cockroach, Periplaneta americana, provides a successful model for the study of legged locomotion. Sensory regulation and the relative importance of sensory feedback vs. central control in animal locomotion are key aspects in our understanding of locomotive behavior. Here we introduce the cockroach model and describe the basic characteristics of the neural generation and control of walking and running in this insect. We further provide a brief overview of some recent studies, including mathematical modeling, which have contributed to our knowledge of sensory control in cockroach locomotion. We focus on two sensory mechanisms and sense organs, those providing information related to loading and unloading of the body and the legs, and leg-movement-related sensory receptors, and present evidence for the instrumental role of these sensory signals in inter-leg locomotion control. We conclude by identifying important open questions and indicate future perspectives.

Keywords

Periplaneta americana Proprioception Campaniform sensilla Chordotonal organ Feedback control 

Notes

Acknowledgments

This work was supported by BSF grant No. 2011059 (AA and PH), and by NSF-CRCNS DMS-1430077 and Princeton University under the J. Insley Blair Pyne Fund (EC-F and PH).

References

  1. Akay T, Haehn S, Schmitz J, Büschges A (2004) Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg. J Neurophysiol 92(1):42–51PubMedCrossRefGoogle Scholar
  2. Altman J (1982) The role of sensory inputs in insect flight motor pattern generation. Trends Neurosci 5:257–258CrossRefGoogle Scholar
  3. Arshavsky YI (2003) Cellular and network properties in the functioning of the nervous system: from central pattern generators to cognition. Brain Res Rev 41:229–267PubMedCrossRefGoogle Scholar
  4. 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(10):921–926PubMedCrossRefGoogle Scholar
  5. Bergman SJ, Pearson KG (1968) Inhibition in cockroach muscle. J Physiol 195(2):22P–23PPubMedGoogle Scholar
  6. Borgmann A, Hooper SL, Büschges A (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):2972–2983PubMedCrossRefGoogle Scholar
  7. Brodfuehrer PD, Fourtner CR (1983) Reflexes evoked by the femoral and coxal chordotonal organs in the cockroach, Periplaneta americana. Comp Biochem Physiol A 74:169–174CrossRefGoogle Scholar
  8. Bucher D (2009) Central pattern generators. Ency Neurosci, pp 691–700Google Scholar
  9. Büschges A (2005) Sensory control and organization of neural networks mediating coordination of multisegmental organs for locomotion. J Neurophysiol 93(3):1127–1135PubMedCrossRefGoogle Scholar
  10. Büschges A, Schmitz J, Bässler U (1995) Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine. J Exp Biol 198:435–456Google Scholar
  11. Büschges A, Akay T, Gabriel J, Schmidt J (2007) Organizing network action for locomotion: insights from studying insect walking. Brain Res Rev 57:162–171PubMedCrossRefGoogle Scholar
  12. Büschges A, Scholz H, El Manira A (2011) New moves in motor control. Curr Biol 21(13):R513–R524PubMedCrossRefGoogle Scholar
  13. Chiel HJ, Ting LH, Ekeberg O, Hartmann MJ (2009) The brain in its body: motor control and sensing in a biomechanical context. J Neurosci 29:12807–12814PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cocatre-Zilgien JH, Delcomyn F (1990) Fast axon activity and the motor pattern in cockroach legs during swimming. Physiol Entomol 15(4):385–392CrossRefGoogle Scholar
  15. Cocatre-Zilgien JH, Delcomyn F (1999) Modeling stress and strain in an insect leg for simulation of campaniform sensilla responses to external forces. Biol Cyber 81:149–160CrossRefGoogle Scholar
  16. Couzin-Fuchs E, Kiemel T, Gal O, Ayali A, Holmes P (2015) Intersegmental coupling and recovery from perturbations in freely-running cockroaches. J Exp Biol (in press)Google Scholar
  17. Cowan NJ, Fortune ES (2007) The critical role of locomotion mechanics in decoding sensory systems. J Neurosci 27:1123–1128PubMedCrossRefGoogle Scholar
  18. Delcomyn F (1971) The locomotion of the cockroach Periplaneta americana. J Exp Biol 54(2):443–452Google Scholar
  19. Delcomyn F (1987) Motor activity during searching and walking movements of cockroach legs. J Exp Biol 133:111–120PubMedGoogle Scholar
  20. Delcomyn F (1991a) 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 156:483–502PubMedGoogle Scholar
  21. Delcomyn F (1991b) 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 156:503–517PubMedGoogle Scholar
  22. Dickinson MH, Farley CT, Full RJ, Koehl MAR, Kram R, Lehman S (2000) How animals move: an integrative view. Science 288:100–106PubMedCrossRefGoogle Scholar
  23. Field LH, Matheson T (1998) Chordotonal organs of insects. Adv Insect Physiol 27:1–228CrossRefGoogle Scholar
  24. French AS, Sanders EJ (1979) The mechanism of sensory transduction in the sensilla of the trochanteral hair plate of the cockroach, Periplaneta americana. Cell Tissue Res 198:159–174PubMedCrossRefGoogle Scholar
  25. Friesen WO, Cang J (2001) Sensory and central mechanisms control inter-segmental coordination. Curr Opin Neurobiol 11(6):678–683PubMedCrossRefGoogle Scholar
  26. Fuchs E, Holmes P, Kiemel T, Ayali A (2011) Inter-segmental coordination of cockroach locomotion: adaptive control of centrally coupled pattern generator circuits. Front Neural Circ 4:125Google Scholar
  27. Fuchs E, Holmes P, David I, Ayali A (2012) Proprioceptive feedback reinforces centrally generated stepping patterns in the cockroach. J Exp Biol 215(11):1884–1891PubMedCrossRefGoogle Scholar
  28. Full RJ, Koditschek DE (1999) Templates and anchors: neuromechanical hypotheses of legged locomotion on land. J Exp Biol 202:3325–3332PubMedGoogle Scholar
  29. Full RJ, Tu MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. J Exp Biol 156(1):215–231PubMedGoogle Scholar
  30. Gao Y, Chen WH, Lu Z (2011) Kinematics analysis and experiment of a cockroach-like robot. J Shanghai Jiaotong Univ (Science) 16:71–77CrossRefGoogle Scholar
  31. Ghigliazza R, Holmes P (2004) A minimal model of a central pattern generator and motoneurons for insect locomotion. SIAM J Appl Dyn Syst 3(4):671–700CrossRefGoogle Scholar
  32. Gorelkin VS, SeverinaI Yu, Isavnina IL (2013) Functional role of leg receptors of the cockroach Periplaneta americana in the system of walking control. J Evol Biochem Physiol 49(3):348–352 (Original Russian Text © V.S. Gorelkin, I.Yu. Severina, I.L. Isavnina, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2012, Vol.48, No. 6,pp. 568–572.)CrossRefGoogle Scholar
  33. Graham D (1985) Pattern and control of walking in insects. Adv Insect Physiol 18:31–140CrossRefGoogle Scholar
  34. Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex integration. Physiol Rev 55:247–304PubMedGoogle Scholar
  35. Guo P, Ritzmann RE (2013) Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J Exp Biol 216(6):992–1002PubMedCrossRefGoogle Scholar
  36. Guthrie DM, Tindall AR (1968) The biology of the cockroach. Edward Arnold, LondonGoogle Scholar
  37. Holmes P, Full RJ, Koditschek DE, Guckenheimer J (2006) The dynamics of legged locomotion: models, analyses and challenges. SIAM Rev 48:207–304CrossRefGoogle Scholar
  38. Hooper SL (2000) Central pattern generators. Curr Biol 10(5):R176–R179PubMedCrossRefGoogle Scholar
  39. Hughes GM (1952) The co-ordination of insect movements: I The walking movements of insects. J Exp Biol 29:267–285Google Scholar
  40. Iles JF, Pearson KG (1969) Central patterning of motoneuronal activity in the cockroach. J Physiol 204(2):54P–55PPubMedGoogle Scholar
  41. Iles JF, Pearson KG (1971) Coxal depressor muscles of the cockroach and the role of peripheral inhibition. J Exp Biol 55:131–164Google Scholar
  42. Jindrich D, Full RJ (2002) Dynamic stabilization of rapid hexapedal locomotion. J Exp Biol 205:2803–2823PubMedGoogle Scholar
  43. Kaliyamoorthy S, Zill SN, Quinn RD (2005) Force sensors in hexapod locomotion. Int J Robotics Res 24:563–574CrossRefGoogle Scholar
  44. Kingsley DA, Quinn RD, Ritzmann RE (2006) A cockroach inspired robot with artificial muscles. In: Intelligent robots and systems, 2006 IEEE/RSJ international conference on (pp 1837–1842). IEEEGoogle Scholar
  45. Krämer K, Markl H (1978) Flight inhibition on ground contact in the American cockroach, Periplaneta americana. I. Contact receptors and a model for their central connections. J Insect Physiol 24:577–586CrossRefGoogle Scholar
  46. Kubow TM, Full RJ (1999) The role of the mechanical system in control: a hypothesis of self-stabilization in hexapedal runners. Philos Trans R Soc Lond B 354:849–861CrossRefGoogle Scholar
  47. Kukillaya R, Proctor J, Holmes P (2009) Neuromechanical models for insect locomotion: stability, maneuverability, and proprioceptive feedback. Chaos 19(2):026107PubMedCrossRefGoogle Scholar
  48. Larsen GS, Frazier SF, Fish SE, Zill SN (1995) Effects of load inversion in cockroach walking. J Comp Physiol A 176:229–238PubMedCrossRefGoogle Scholar
  49. Ludwar BCh, Goritz ML, Schmidt J (2005) Intersegmental coordination of walking movements in stick insects. J Neurophysiol 93:1255–1265PubMedCrossRefGoogle Scholar
  50. Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986–R996PubMedCrossRefGoogle Scholar
  51. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687–717PubMedGoogle Scholar
  52. Mendes CS, Bartos I, Akay T, Márka S, Mann RS (2013) Quantification of gait parameters in freely walking wild type and sensory deprived Drosophila melanogaster. ELife 2:e00231PubMedCentralPubMedGoogle Scholar
  53. Mu L, Ritzmann RE (2008a) Interaction between descending input and thoracic reflexes for joint coordination in cockroach: I Descending influence on thoracic sensory reflexes. J Comp Physiol A 194(3):283–298CrossRefGoogle Scholar
  54. Mu L, Ritzmann RE (2008b) Interaction between descending input and thoracic reflexes for joint coordination in cockroach. II Comparative studies on tethered turning and searching. J Comp Physiol A 194(3):299–312CrossRefGoogle Scholar
  55. Noah JA, Quimby L, Frazier SF, Zill SN (2001) Force receptors in cockroach walking reconsidered, discharges of proximal tibial campaniform sensilla when body load is altered. J Comp Physiol A 187:769–784PubMedCrossRefGoogle Scholar
  56. Noah JA, Quimby L, Frazier SF, Zill SN (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 190:201–215CrossRefGoogle Scholar
  57. Okada R, Ikeda J, Mizunami M (1999) Sensory responses and movement-related activities in extrinsic neurons of the cockroach mushroom bodies. J Comp Physiol A 185(2):115–129CrossRefGoogle Scholar
  58. Pearson KG (1972) Central programming and reflex control of walking in the cockroach. J Exp Biol 56(1):173–193Google Scholar
  59. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Ann Rev Neurosci 16:265–297PubMedCrossRefGoogle Scholar
  60. Pearson KG (2004) Generating the walking gait: role of sensory feedback. Prog Brain Res 143:123–129PubMedCrossRefGoogle Scholar
  61. Pearson KG, Bergman SJ (1969) Common inhibitory motoneurones in insects. J Exp Biol 50(2):445–471PubMedGoogle Scholar
  62. Pearson KG, Iles JF (1970) Discharge patterns of coxal levator and depressor motoneurones of the cockroach Periplaneta americana. J Exp Biol 52(1):139–165PubMedGoogle Scholar
  63. Pearson KG, Iles JF (1973) Nervous mechanisms underlying intersegmental co-ordination of leg movements during walking in the cockroach. J Exp Biol 58:725–744Google Scholar
  64. Pearson KG, Wong RK, Fourtner CR (1976) Connexions between hair-plate afferents and motoneurones in the cockroach leg. J Exp Biol 64(1):251–266PubMedGoogle Scholar
  65. Pearson KG, Ekeberg Ö, Büschges A (2006) Assessing sensory function in locomotor systems using neuro-mechanical simulations. Trends Neurosci 29(11):625–631PubMedCrossRefGoogle Scholar
  66. Pfeifer R, Lungarella M, Iida F (2007) Self-organization, embodiment, and biologically inspired robotics. Science 318:1088–1093PubMedCrossRefGoogle Scholar
  67. Pringle JWS (1940) Reflex mechanism of the insect leg. J Exp Biol 17:8–17Google Scholar
  68. Proctor J, Holmes P (2010) Reflexes and preflexes: on the role of sensory feedback on rhythmic patterns in insect locomotion. Biol Cybern 102:513–531PubMedCrossRefGoogle Scholar
  69. Proctor J, Kukillaya RP, Holmes P (2010) A phase-reduced neuro-mechanical model for insect locomotion: feedforward stability and proprioceptive feedback. Philos Trans R Soc Lond A368:5087–5104CrossRefGoogle Scholar
  70. Puhl JG, Mesce KA (2010) Keeping it together: mechanisms of inter-segmental coordination for a flexible locomotor behavior. J Neurosci 30(6):2373–2383PubMedCentralPubMedCrossRefGoogle Scholar
  71. Reingold SC, Camhi JM (1977) A quantitative analysis of rhythmic leg movements during three different behaviors in the cockroach. J Insect Physiol 23:1407–1420CrossRefGoogle Scholar
  72. Revzen S, Burden SA, Moore TY, Mongeau JM, Full RJ (2013) Instantaneous kinematic phase reflects neuromechanical response to lateral perturbations of running cockroaches. Biol Cybern 107(2):179–200PubMedCrossRefGoogle Scholar
  73. Ridgel AL, Ritzmann RE (2005) Effects of neck and circumoesophageal connective lesions on posture and locomotion in the cockroach. J Comp Physiol A 191:559–573Google Scholar
  74. Ridgel AL, Frazier SF, DiCaprio RA, Zill SN (1999) Active signaling of leg loading and unloading in the cockroach. J Neurophysiol 81:1432–1437PubMedGoogle Scholar
  75. Ridgel AL, Frazier SF, DiCaprio RA, Zill SN (2000) Encoding of forces by cockroach tibial campaniform sensilla, implications in dynamic control of posture and locomotion. J Comp Physiol A 186:359–374PubMedCrossRefGoogle Scholar
  76. Ridgel AL, Frazier SF, Zill SN (2001) Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches. J Comp Physiol A 187:405–420PubMedCrossRefGoogle Scholar
  77. Rillich J, Stevenson PA, Pflueger H-J (2013) Flight and walking in locusts: cholinergic co-activation, temporal coupling and its modulation by biogenic amines. PLoS One 8(5):e62899PubMedCentralPubMedCrossRefGoogle Scholar
  78. Ritzmann R, Zill SN (2013) Neuroethology of insect walking. Scholarpedia 8(9):30879CrossRefGoogle Scholar
  79. Schmitt J, Holmes P (2000) Mechanical models for insect locomotion: dynamics and stability in the horizontal plane I. Theory. Biol Cybern 83:501–515PubMedCrossRefGoogle Scholar
  80. Schmitt J, Garcia M, Razo C, Holmes P, Full RJ (2002) Dynamics and stability of legged locomotion in the horizontal plane: a test case using insects. Biol Cybern 86:343–353PubMedCrossRefGoogle Scholar
  81. Schroer RT, Boggess MJ, Bachmann RJ, Quinn RD, Ritzmann RE (2004) Comparing cockroach and whegs robot body motions. In: Robotics and automation, proceedings ICRA’04. 2004 IEEE international conference on robotics and automation (Vol. 4, pp. 3288–3293). IEEEGoogle Scholar
  82. Seipel J, Holmes P, Full RJ (2004) Dynamics and stability of insect locomotion: a hexapedal model for horizontal plane motion. Biol Cybern 91:76–90PubMedCrossRefGoogle Scholar
  83. Skinner FK, Mulloney B (1998) Inter-segmental coordination in invertebrates and vertebrates. Curr Opin Neurobiol 8:725–732PubMedCrossRefGoogle Scholar
  84. Spence AJ, Revzen S, Seipel J, Mullens C, Full RJ (2010) Insects running on elastic surfaces. J Exp Biol 213:1907–1920PubMedCrossRefGoogle Scholar
  85. Sponberg S, Libby T, Mullens CH, Full RJ (2011) Shifts in a single muscle’s control potential of body dynamics are determined by mechanical feedback. Philos Trans R Soc Lond B 366:1606–1620CrossRefGoogle Scholar
  86. Tang TP, Macmillan DL (1986) The effects of sensory manipulation upon interlimb coordination during fast walking in the cockroach. J Exp Biol 125:107–117Google Scholar
  87. Tytell E, Holmes P, Cohen A (2011) Spikes alone do not behavior make: why neuroscience needs biomechanics. Curr Opin Neurobiol 21:816–822PubMedCentralPubMedCrossRefGoogle Scholar
  88. Watson JT, Ritzmann RE, Pollack AJ (2002) Control of climbing behavior in the cockroach, Blaberus discoidalis. II Motor activities associated with joint movement. J Comp Physiol A 188:55–69CrossRefGoogle Scholar
  89. Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471–490Google Scholar
  90. Wong RK, Pearson KG (1976) Properties of the trochanteral hair plate and its function in the control of walking in the cockroach. J Exp Biol 64(1):233–249PubMedGoogle Scholar
  91. Yu X, Friesen WO (2004) Entrainment of leech swimming activity by the ventral stretch receptor. J Comp Physiol A 190:939–949Google Scholar
  92. Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58:185–205PubMedCrossRefGoogle Scholar
  93. Zill SN (1986) A model of pattern generation of cockroach walking reconsidered. J Neurobiol 17:317–328PubMedCrossRefGoogle Scholar
  94. Zill SN, Moran DT (1981a) The exoskeleton and insect proprioception. I. Responses of tibial campaniform sensilla to external and muscle regenerated forces in the American cockroach Periplaneta americana. J Exp Biol 91:1–24Google Scholar
  95. Zill SN, Moran DT (1981b) The exoskeleton and insect proprioception. III. Activity of tibial campaniform sensilla during walking in the American cockroach Periplaneta americana. J Exp Biol 94:57–75Google Scholar
  96. Zill SN, Ridgel AL, DiCaprio RA, Frazier SF (1999) Load signaling by cockroach trochanteral campaniform sensilla. Brain Res 822:271–275PubMedCrossRefGoogle Scholar
  97. Zill SN, Schmitz J, Büschges A (2004) Load sensing and control of posture and locomotion. Arthropod Struct Dev 33:273–286PubMedCrossRefGoogle Scholar
  98. 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 101:2297–2304PubMedCrossRefGoogle Scholar
  99. Zill SN, Keller BR, Chaudhry S, Duke ER, Neff D, Quinn R, Flannigan C (2010) Detecting substrate engagement: responses of tarsal campaniform sensilla in cockroaches. J Comp Physiol A 196(6):407–420CrossRefGoogle Scholar
  100. 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(5):1453–1472PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • A. Ayali
    • 1
    • 2
  • E. Couzin-Fuchs
    • 1
    • 3
  • I. David
    • 1
  • O. Gal
    • 1
  • P. Holmes
    • 3
    • 4
  • D. Knebel
    • 1
    • 2
  1. 1.Department of ZoologyTel Aviv UniversityTel AvivIsrael
  2. 2.Sagol School of NeuroscienceTel Aviv UniversityTel AvivIsrael
  3. 3.Department of Mechanical and Aerospace EngineeringPrinceton UniversityPrincetonUSA
  4. 4.Program in Applied and Computational Mathematics and Princeton Neuroscience InstitutePrinceton UniversityPrincetonUSA

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