Abstract
Sensory feedback from sense organs during animal locomotion can be heavily influenced by an organism’s mechanical structure. In insects, the interplay between sensing and mechanics can be demonstrated in the campaniform sensilla (CS) strain sensors located across the exoskeleton. Leg CS are highly sensitive to the loading state of the limb. In walking, loading is primarily influenced by ground reaction forces (GRF) mediated by the foot, or tarsus. The complex morphology of the tarsus provides compliance, passive and active substrate grip, and an increased moment arm for the GRF, all of which impact leg loading and the resulting CS discharge. To increase the biomimicry of robots we use to study strain feedback during insect walking, we have developed a series of tarsi for our robotic model of a Carausius morosus middle leg. We seek the simplest design that mimics tarsus functionality. Tarsi were designed with varying degrees of compliance, passive grip, and biomimetic structure. We created elastic silicone tarsal joints for several of these models and found that they produced linear stiffness within joint limits across different joint morphologies. Strain gauges positioned in CS locations on the trochanterofemur and tibia recorded strain while the leg stepped on a treadmill. Most, but not all, designs increased axial strain magnitude compared to previous data with no tarsus. Every tarsus design produced positive transversal strain in the tibia, indicating axial torsion in addition to bending. Sudden increases in tibial strain reflected leg slipping during stance. This data show how different aspects of the tarsus may mediate leg loading, allowing us to improve the mechanical biomimicry of future robotic test platforms.
Supported by NSF/DBI NeuroNex 2015317 to NSS, DFG Bu857/125-1 to AB, NSF CRCNS 2113028 to NSS and SNZ, and DFG DI 2907/1-1 (Project number 500615768, grant no. 233886668/GRK1960) to GFD.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Arnold, J.: Adaptive features on the tarsi of cockroaches (Insecta: Dictyoptera). Int. J. Insect. Morphol. 3(3/4), 317–334 (1974). https://doi.org/10.1016/j.ymeth.2019.07.013
Bässler, U.: Neural Basis of Elementary Behavior in Stick Insects. Springer, Berlin (1983). https://doi.org/10.1007/978-3-642-68813-3_6
Bennemann, M.: Biomimicry of the adhesive organs of stick insects (Carausius morosus). Ph.D. thesis, RWTH Aachen University (2015)
Bidaye, S.S., Bockemühl, T., Büschges, A.: Six-legged walking in insects: how CPGs, peripheral feedback, and descending signals generate coordinated and adaptive motor rhythms. J. Neurophysiol. 119(2) (2018). https://doi.org/10.1152/jn.00658.2017
Buschmann, T., Ewald, A., von Twickel, A., Büschges, A.: Controlling legs for locomotion-insights from robotics and neurobiology. Bioinspir. Biomim. 10(4), 41001 (2015). https://doi.org/10.1088/1748-3190/10/4/041001
Bußhardt, P., Gorb, S.N., Wolf, H.: Activity of the claw retractor muscle in stick insects in wall and ceiling situations. J. Exp. Biol. 214(10), 1676–1684 (2011). https://doi.org/10.1242/jeb.051953
Bußhardt, P., Wolf, H., Gorb, S.N.: Adhesive and frictional properties of tarsal attachment pads in two species of stick insects (Phasmatodea) with smooth and nubby euplantulae. Zoology 115(3), 135–141 (2012). https://doi.org/10.1016/j.zool.2011.11.002, http://dx.doi.org/10.1016/j.zool.2011.11.002
van Casteren, A., Codd, J.R.: Foot morphology and substrate adhesion in the Madagascan hissing cockroach, Gromphadorhina portentosa. J. Insect. Sci. 10(1), 1–12 (2010). https://doi.org/10.1673/031.010.4001
Chiel, H.J., Beer, R.D.: The brain has a body: adaptive behavior emerges from interactions of nervous system, body and environment. Trends Neurosci. 20(12), 553–557 (1997). https://doi.org/10.1016/S0166-2236(97)01149-1
Cignoni, P., Callieri, M., Corsini, M., Dellepiane, M., Ganovelli, F., Ranzuglia, G.: MeshLab: an open-source mesh processing tool. In: Scarano, V., Chiara, R.D., Erra, U. (eds.) Eurographics Italian Chapter Conference. The Eurographics Association (2008). https://doi.org/10.2312/LocalChapterEvents/ItalChap/ItalianChapConf2008/129-136
Clemente, C.J., Dirks, J.H., Barbero, D.R., Steiner, U., Federle, W.: Friction ridges in cockroach climbing pads: Anisotropy of shear stress measured on transparent, microstructured substrates. J. Comp. Physiol. A 195(9), 805–814 (2009). https://doi.org/10.1007/s00359-009-0457-0
Cruse, H., Bartling, C.: Movement of joint angles in the legs of a walking insect, Carausius morosus. J. Insect Physiol. 41(9), 761–771 (1995). https://doi.org/10.1016/0022-1910(95)00032-P
Delcomyn, F.: Activity and directional sensitivity of leg campaniform sensilla in a stick insect. J. Comp. Physiol. A 168(1), 113–119 (1991). https://doi.org/10.1007/BF00217109
Delcomyn, F., Nelson, M.E., Cocatre-Zilgien, J.H.: Sense organs of insect legs and the selection of sensors for agile walking robots. Int. J. Robot. Res. 15(2), 113–127 (1996). https://doi.org/10.1177/027836499601500201
Dinges, G.F., Bockemühl, T., Iacoviello, F., Shearing, P.R., Büschges, A., Blanke, A.: Ultra high-resolution biomechanics suggest that substructures within insect mechanosensors decisively affect their sensitivity. J. Roy. Soc. Interface 19(190), 20220102 (2022). https://doi.org/10.1098/rsif.2022.0102
Frazier, S.F., et al.: Elasticity and movements of the cockroach tarsus in walking. J. Comp. Physiol. A 185(2), 157–172 (1999). https://doi.org/10.1007/s003590050374
Goldsmith, C.A., Szczecinski, N.S., Quinn, R.D.: Neurodynamic modeling of the fruit fly Drosophila melanogaster. Bioinspir. Biomim. 15(6) (2020). https://doi.org/10.1088/1748-3190/ab9e52
Goldsmith, C., Quinn, R.D., Szczecinski, N.S.: Investigating the role of low level reinforcement reflex loops in insect locomotion. Bioinspir. Biomim. 16, 065008 (2021). https://doi.org/10.1088/1748-3190/ac28ea
Gorb, S.N.: Design of insect unguitractor apparatus. J. Morphol. 230(2), 219–230 (1996). https://doi.org/10.1002/(SICI)1097-4687(199611)230:2<219::AID-JMOR8>3.0.CO;2-B
Harris, C.M., Szczecinski, N.S., Büschges, A., Zill, S.N.: Sensory signals of unloading in insects are tuned to distinguish leg slipping from load variations in gait: experimental and modeling studies. J. Neurophysiol. 128(5), 790–807 (2022). https://doi.org/10.1152/jn.00285.2022
Kohsaka, H., Nose, A.: Optogenetics in Drosophila. Adv. Exp. Med. Biol. 1293, 309–320 (2021). https://doi.org/10.1016/j.ymeth.2019.07.013
Larsen, G.S., Frazier, S.F., Zill, S.N.: The tarso-pretarsal chordotonal organ as an element in cockroach walking. J. Comp. Physiol. A 180(6), 683–700 (1997). https://doi.org/10.1007/s003590050083
Liessem, S., et al.: Behavioral state-dependent modulation of insulin-producing cells in Drosophila. Curr. Biol. 33(3), 449-463.e5 (2023). https://doi.org/10.1016/j.cub.2022.12.005
Manoonpong, P., et al.: Insect-inspired robots: bridging biological and artificial systems. Sensors 21(22), 1–44 (2021). https://doi.org/10.3390/s21227609
Merritt, D.J., Murphey, R.K.: Projections of leg proprioceptors within the CNS of the fly phormia in relation to the generalized insect ganglion. J. Comp. Neurol. 322(1), 16–34 (1992). https://doi.org/10.1002/cne.903220103
Moran, D.T., Chapman, K.M., Ellis, R.A.: The fine structure of cockroach campaniform sensilla. J. Cell Biol. 48(1), 155–173 (1971). https://doi.org/10.1083/jcb.48.1.155
Noah, A.J., Quimby, L., Frazier, F.S., Zill, S.N.: Force detection in cockroach walking reconsidered: discharges of proximal tibial campaniform sensilla when body load is altered. J. Comp. Physiol. - Sens. Neural Behav. Physiol. 187(10), 769–784 (2001). https://doi.org/10.1007/s00359-001-0247-9
Pfeifer, R., Iida, F., Gómez, G.: Morphological computation for adaptive behavior and cognition. Int. Congr. Ser. 1291, 22–29 (2006). https://doi.org/10.1016/j.ics.2005.12.080
Radnikow, G., Bässler, U.: 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(1), 87–99 (1991). https://doi.org/10.1242/jeb.157.1.87
Ridgel, A.L., Frazier, S.F., Zill, S.N.: Dynamic responses of tibial campaniform sensilla studied by substrate displacement in freely moving cockroaches. J. Comp. Physiol. A 187(5), 405–420 (2001). https://doi.org/10.1007/s003590100213
Ritzmann, R.E., Quinn, R.D., Watson, J.T., Zill, S.N.: Insect walking and biorobotics: a relationship with mutual benefits. Bioscience 50(1), 23–33 (2000). https://doi.org/10.1641/0006-3568(2000)050[0023:IWABAR]2.3.CO;2
Scheffer, L.K., et al.: A connectome and analysis of the adult Drosophila central brain. eLife 9, 1–74 (2020). https://doi.org/10.7554/ELIFE.57443
Szczecinski, N.S., Dallmann, C.J., Quinn, R.D., Zill, S.N.: A computational model of insect campaniform sensilla predicts encoding of forces during walking. Bioinspir. Biomim. 16(6) (2021). https://doi.org/10.1088/1748-3190/ac1ced
Tajiri, R., Misaki, K., Yonemura, S., Hayashi, S.: Joint morphology in the insect leg: evolutionary history inferred from Notch loss-of-function phenotypes in Drosophila. Development 138(21), 4621–4626 (2011). https://doi.org/10.1242/dev.067330
Tran-Ngoc, P.T., Lim, L.Z., Gan, J.H., Wang, H., Vo-Doan, T.T., Sato, H.: A robotic leg inspired from an insect leg. Bioinspir. Biomim. 17(5) (2022). https://doi.org/10.1088/1748-3190/ac78b5
Zill, S.N., Moran, D.T.: 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 (1981)
Zill, S., Schmitz, J., Büschges, A.: Load sensing and control of posture and locomotion. Arthropod. Struct. Dev. 33(3), 273–286 (2004). https://doi.org/10.1016/j.asd.2004.05.005
Zill, S.N., Büschges, A., Schmitz, J.: Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus. J. Comp. Physiol. A 197(8), 851–867 (2011). https://doi.org/10.1007/s00359-011-0647-4
Zill, S.N., Chaudhry, S., Büschges, A., Schmitz, J.: Force feedback reinforces muscle synergies in insect legs. Arthropod. Struct. Dev. 44(6), 541–553 (2015). https://doi.org/10.1016/j.asd.2015.07.001
Zill, S.N., Chaudhry, S., Exter, A., Büschges, A., Schmitz, J.: Positive force feedback in development of substrate grip in the stick insect tarsus. Arthropod. Struct. Dev. 43(5), 441–455 (2014). https://doi.org/10.1016/j.asd.2014.06.002
Zill, S.N., Ridgel, A.L., DiCaprio, R.A., Frazier, S.: Load signalling by cockroach trochanteral campaniform sensilla. Brain Res. 822(1), 271–275 (1999). https://doi.org/10.1016/S0006-8993(99)01156-7
Zyhowski, W.P., Zill, S.N., Szczecinski, N.S.: Adaptive load feedback robustly signals force dynamics in robotic model of Carausius morosus stepping. Front. Neurorobot. 17(January) (2023). https://doi.org/10.3389/fnbot.2023.1125171
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this paper
Cite this paper
Goldsmith, C.A., Zyhowski, W.P., Büschges, A., Zill, S.N., Dinges, G.F., Szczecinski, N.S. (2023). Effects of Tarsal Morphology on Load Feedback During Stepping of a Robotic Stick Insect (Carausius Morosus) Limb. In: Meder, F., Hunt, A., Margheri, L., Mura, A., Mazzolai, B. (eds) Biomimetic and Biohybrid Systems. Living Machines 2023. Lecture Notes in Computer Science(), vol 14157. Springer, Cham. https://doi.org/10.1007/978-3-031-38857-6_32
Download citation
DOI: https://doi.org/10.1007/978-3-031-38857-6_32
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-38856-9
Online ISBN: 978-3-031-38857-6
eBook Packages: Computer ScienceComputer Science (R0)