Abstract
The peripheral auditory system of lizards has been extensively studied, because of its remarkable directionality. In this paper, we review the research that has been performed on this system using a biorobotic approach. The various robotic implementations developed to date, both wheeled and legged, of the auditory model exhibit strong phonotactic performance for two types of steering mechanisms—a simple threshold decision model and Braitenberg sensorimotor cross-couplings. The Braitenberg approach removed the need for a decision model, but produced relatively inefficient robot trajectories. Introducing various asymmetries in the auditory model reduced the efficiency of the robot trajectories, but successful phonotaxis was maintained. Relatively loud noise distractors degraded the trajectory efficiency and above-threshold noise resulted in unsuccessful phonotaxis. Machine learning techniques were applied to successfully compensate for asymmetries as well as noise distractors. Such techniques were also successfully used to construct a representation of auditory space, which is crucial for sound localisation while remaining stationary as opposed to phonotaxis-based localisation. The peripheral auditory model was furthermore found to adhere to an auditory scaling law governing the variation in frequency response with respect to physical ear separation. Overall, the research to date paves the way towards investigating the more fundamental topic of auditory metres versus auditory maps, and the existing robotic implementations can act as tools to compare the two approaches.
Similar content being viewed by others
References
Albus J (1971) A theory of cerebellar function. Math Biosci 10(1–2):25–61
Albus J (1975) A new approach to manipulator control: the cerebellar model articulation controller (CMAC). J Dyn Syst Meas Control 97(3):220–227
Albus J (1979) Mechanisms of planning and problem solving in the brain. Math Biosci 45(3–4):247–293
Braitenberg V (1984) Vehicles: experiments in synthetic psychology. MIT Press, Bradford Books, Cambridge
Carr C, Christensen-Dalsgaard J, Bierman H (2016) Coupled ears in lizards and crocodilians. Biol Cybern. doi:10.1007/s00422-016-0698-2
Christensen-Dalsgaard J (2005) Directional hearing in nonmammalian tetrapods. In: Popper A, Fay R (eds) Sound source localization, Springer handbook of auditory research, vol 25. Springer, New York, pp 67–123
Christensen-Dalsgaard J (2011) Vertebrate pressure-gradient receivers. Hear Res 273(1–2):37–45
Christensen-Dalsgaard J, Manley G (2005) Directionality of the lizard ear. J Exp Biol 208(6):1209–1217
Christensen-Dalsgaard J, Manley G (2008) Acoustical coupling of lizard eardrums. J Assoc Res Otolaryngol 9(4):407–416
Christensen-Dalsgaard J, Tang Y, Carr C (2011) Binaural processing by the gecko auditory periphery. J Neurophysiol 105(5):1992–2004
Daan S, Belterman T (1968) Lateral bending in locomotion of some lower tetrapods. Proc Ned Akad Wetten Ser C 71:245–266
Fletcher N (1992) Acoustic systems in biology. Oxford University Press, Oxford
Fletcher N, Thwaites S (1979) Physical models for the analysis of acoustical systems in biology. Q Rev Biophys 12(1):25–65
Heffner HE, Heffner RS (2008) High-frequency hearing. In: Basbaum AI, Kaneko A, Shepherd GM, Westheimer G (eds) The senses: a comprehensive reference, vol 3. Audition. Academic Press, San Diego, pp 55–60
Karakasiliotis K, Ijspeert A (2009) Analysis of the terrestrial locomotion of a salamander robot. In: IEEE/RSJ international conference on intelligent robots and systems, 2009. IROS 2009. pp 5015–5020. doi:10.1109/IROS.2009.5354220
Klump G (2000) Sound localization in birds. In: Dooling R, Fay R, Popper A (eds) Comparative hearing: birds and reptiles, Springer handbook of auditory research, vol 13. Springer, Berlin, pp 249–307
Masseck O, Röll B, Hoffmann KP (2008) The optokinetic reaction in foveate and afoveate geckos. Vis Res 48(6):765–772
Michelsen A (1998) Biophysics of sound localization in insects. In: Hoy R, Popper A, Fay R (eds) Comparative hearing: insects, Springer handbook of auditory research, vol 10. Springer, Berlin, pp 18–62
Michelsen A, Popov A, Lewis B (1994) Physics of directional hearing in the cricket gryllus bimaculatus. J Comp Physio Neuroethol Sens Neural Behav Physiol 175(2):153–164
Rañó I (2012) A model and formal analysis of braitenberg vehicles 2 and 3. In: 2012 IEEE international conference on robotics and automation (ICRA), pp 910–915
Rañó I (2012) An introduction to the analysis of braitenberg vehicles 2 and 3 using phase plane portrait. In: Ziemke T, Balkenius C, Hallam J (eds) From animals to animats 12, Lecture notes in computer science, vol 7426, Springer, Berlin, pp 23–32
Reilly S, Delancey M (1997) Sprawling locomotion in the lizard sceloporus clarkii: quantitative kinematics of a walking trot. J Exp Biol 200(4):753–765
Ritter D (1992) Lateral bending during lizard locomotion. J Exp Biol 173(1):1–10
Roos P (1964) Lateral bending in newt locomotion. Proc Ned Akad Wetten Ser C 67:223–232
Shaikh D (2012) Exploring a robotic model of the lizard peripheral auditory system. Ph.D. thesis, University of Southern Denmark
Shaikh D, Hallam J, Christensen-Dalsgaard J (2009) Control of a braitenberg lizard in a phonotaxis task with decision models. In: Kyriacou T, Nehmzow U, Melhuish C, Witkowski M (eds) Technical report series: proceedings of towards autonomous robotic systems. University of Ulster, Intelligent Systems Research Centre, University of Ulster, pp 48–54
Shaikh D, Hallam J, Christensen-Dalsgaard J, Zhang L (2009) A braitenberg lizard: continuous phonotaxis with a lizard ear model. In: IWINAC ’09: proceedings of the 3rd international work-conference on the interplay between natural and artificial computation, Springer, Berlin, Heidelberg, pp 439–448. doi:10.1007/978-3-642-02267-8_47
Shaikh D, Hallam J, Christensen-Dalsgaard J (2010) Modifying directionality through auditory system scaling in a robotic lizard. In: From animals to animats 11: 11th international conference on simulation of adaptive behavior, SAB 2010, Paris-Clos Lucé, France, August 25–28, 2010. Proceedings, vol 6226, pp 82–92
Shaikh D, Hallam J Christensen-Dalsgaard J (2011) Learning to localize sound with a lizard ear model, presented at the International workshop for bio-inspired robots. Nantes, France 6–8 April 2011
Shaikh D, Hallam J, Christensen-Dalsgaard J, Ijspeert A (2011) Combining bio-inspired sensing with bio-inspired locomotion. In: The 5th International symposium on adaptive motion in animals and machines (AMAM 2011), pp 27–28
Stecker GC, Middlebrooks J (2003) Distributed coding of sound locations in the auditory cortex. Biol Cybern 89(5):341–349
Wever E (1978) The reptile ear: its structure and function. princeton University Press, Princeton
Zhang L (2009) Modelling directional hearing in lizards. Ph.D. thesis, Maersk Mc-Kinney Moller Institute, Faculty of Engineering, University of Southern Denmark
Zhang L, Hallam J, Christensen-Dalsgaard J (2006) Modelling the peripheral auditory system of lizards. In: Nolfi S, Baldassarre G, Calabretta R, Hallam J, Marocco D, Meyer J, Miglino O, Parisi D (eds) From Animals to animats 9, Lecture notes in computer science, vol 4095, Springer, Berlin, pp 65–76
Author information
Authors and Affiliations
Corresponding author
Additional information
This article belongs to a Special Issue on Internally Coupled Ears (ICE).
Rights and permissions
About this article
Cite this article
Shaikh, D., Hallam, J. & Christensen-Dalsgaard, J. From “ear” to there: a review of biorobotic models of auditory processing in lizards. Biol Cybern 110, 303–317 (2016). https://doi.org/10.1007/s00422-016-0701-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-016-0701-y