Journal of Comparative Physiology A

, Volume 192, Issue 9, pp 927–940 | Cite as

On the barn owl’s visual pre-attack behavior: I. Structure of head movements and motion patterns

  • Shay Ohayon
  • Robert F. van der Willigen
  • Hermann Wagner
  • Igor Katsman
  • Ehud Rivlin
Original Paper

Abstract

Barn owls exhibit a rich repertoire of head movements before taking off for prey capture. These movements occur mainly at light levels that allow for the visual detection of prey. To investigate these movements and their functional relevance, we filmed the pre-attack behavior of barn owls. Off-line image analysis enabled reconstruction of all six degrees of freedom of head movements. Three categories of head movements were observed: fixations, head translations and head rotations. The observed rotations contained a translational component. Head rotations did not follow Listing’s law, but could be well described by a second-order surface, which indicated that they are in close agreement with Donder’s law. Head translations did not contain any significant rotational components. Translations were further segmented into straight-line and curved paths. Translations along an axis perpendicular to the line of sight were similar to peering movements observed in other animals. We suggest that these basic motion elements (fixations, head rotations, translations along a straight line, and translation along a curved trajectory) may be combined to form longer and more complex behavior. We speculate that these head movements mainly underlie estimation of distance during prey capture.

Keywords

Motion parallax Peering Movement Motor Motor primitive 

Abbreviation

3D

Three-dimensional

Notes

Acknowledgements

We would like to thank the coordinator of the Bursary program for Israeli students, at the Center of North Rhine-Westphalia, Dr. Arne Claussen, who made Shay Ohayon’s visit to Aachen possible. The experimental procedures were approved by the Regierungspräsidium Köln.

References

  1. Bizzi E, Giszter S, Loeb E, Mussa-Ivaldi F, Salteil P (1995) Modular organization of motor behavior in the frog’s spinal cord. Trends Neurosci 18:442–446PubMedCrossRefGoogle Scholar
  2. Bruss AR, Horn BKP (1983) Passive navigation. Comput Vis Graph 21:3–20Google Scholar
  3. Campbell LW, Bobick A (1995) Recognition of human body motion using phase space constraints. In: International conference on computer and vision, Cambridge, pp 624–630Google Scholar
  4. Collett TS (1978) Peering—a locust behaviour pattern for obtaining motion parallax information. J Exp Biol 76:237–241Google Scholar
  5. Crawford JD, Martinez-Trujillo JC, Klier EM (2003) Neural control of three-dimensional eye and head movements. Curr Opin Neurobiol 13:655–662PubMedCrossRefGoogle Scholar
  6. Du Lac S, Knudsen EI (1990) Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63:131–146PubMedGoogle Scholar
  7. Glenn B, Vilis T (1992) Violations of Listing’s law after large eye and head gaze shifts. J Neurophysiol 68:309–318PubMedGoogle Scholar
  8. Goldengerg R, Kimmel R, Rivlin E, Rudzsky M (2005) Behavior classification by eigen decomposition of periodic motions. Pattern Recognit 38:1033–1043CrossRefGoogle Scholar
  9. Haker H, Misslisch H, Ott M, Frens MA, Henn V, Hess K, Sandor PS (2003) Three-dimensional vestibular eye and head reflexes of the chameleon: characteristics of gain and phase and effects of eye position on orientation of ocular rotation axes during stimulation in yaw direction. J Comp Physiol A 189:509–517CrossRefGoogle Scholar
  10. Haustein W (1989) Considerations on Listing’s law and the primary position by means of a matrix description of eye position control. Biol Cybern 60:411–420PubMedCrossRefGoogle Scholar
  11. Howard IP (2002) Seeing in depth. Basic mechanisms, vol 1. I Porteous Publishing, OntarioGoogle Scholar
  12. Katsman I, Rivlin E (2003) The mantis head camera (why the praying mantis is so good at catching its prey). In: IEEE international conference on image processing, pp 612–617Google Scholar
  13. Knudsen EI, Blasdel GG, Konishi M (1979) Sound localization by the barn owl (Tyto alba) measured with the search coil technique. J Comp Physiol 133:1–11CrossRefGoogle Scholar
  14. Konczak Jr (2005) On the notion of motor primitives in humans and robots. In: Proceedings of the 5th international workshop on epigenetic robot, Nara, vol 123. Lund University Cognitive Studies, pp 47–54Google Scholar
  15. Kral K (2003) Behavioural–analytical studies of the role of head movements in depth perception in insects, birds and mammals. Behav Processes 64:1–12PubMedCrossRefGoogle Scholar
  16. Kral K, Devetak D (1999) The visual orientation strategies of Mantis religiosa and empusafasiata reflect differences in the structure of their visual surroundings. J Insect Behav 12:737–752CrossRefGoogle Scholar
  17. Kral K, Poteser M (1997) Motion parallax as a source of distance information in locusts and mantids. J Insect Behav 10:145–163Google Scholar
  18. Lewis MA, Nelson ME (1998) Look before you leap: peering behavior for depth perception. In: Proc 5 Simul Adapt Behav, pp 98–103Google Scholar
  19. Martin GR (1977) Absolute visual threshold and scotopic spectral sensitivity in the tawny owl (Strix aluco). Nature 268:636–638PubMedCrossRefGoogle Scholar
  20. Martin GR, Katzir G (1999) Visual fields in short-toed eagles (Circaetus gallicus (Accipitridae)) and the function of binocularity in birds. Brain Behav Evol 53:55–66PubMedCrossRefGoogle Scholar
  21. Masino T, Knudsen EI (1990) Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl. Nature 345:434–437PubMedCrossRefGoogle Scholar
  22. Masino T, Knudsen EI (1993) Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. J Neurosci 13:351–370PubMedGoogle Scholar
  23. Medendorp WP, Melis BJM, Gielen CCAM, van Gisbergen JAM (1998) Off-centric rotation axes in natural head movements: implications for vestibular reafference and kinematic redundancy. J Neurophysiol 79:2025–2039PubMedGoogle Scholar
  24. Moeslund TB, Reng L, Granum E (2005) Finding motion primitives in human body gestures. Gesture Workshop 2005, Berder Island, pp 31–33Google Scholar
  25. Mussa-Ivaldi F, Bizzi E (2000) Motor learning through the combination of primitives. Philos Trans R Soc Lond B Biol Sci 355:1755–1769PubMedCrossRefGoogle Scholar
  26. Perner P (2001) Motion tracking of animals for behavior analysis. Lect Notes Comput Sci 2059:779–786Google Scholar
  27. Perona P, Malik J (1990) Scale-space and edge detection using anisotropic diffusion. IEEE Trans Pattern Anal Mach Intell 12:629–639CrossRefGoogle Scholar
  28. Pressley A (2001) Elementary differential geometry. Springer Undergraduate Mathematics Series. ISBN: 1-85233-152-6Google Scholar
  29. Robinson D (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145PubMedGoogle Scholar
  30. Saberi K, Farahbod H, Konishi M (1998) How do owls localize interaurally phase-ambiguous signals? Proc Natl Acad Sci USA 95:6465–6468PubMedCrossRefGoogle Scholar
  31. Sobel EC (1990) The locust’s use of motion parallax to measure distance. J Comp Physiol A 167:579–588PubMedCrossRefGoogle Scholar
  32. Steinbach MJ, Money KE (1973) Eye movements of the owl. Vision Res 13:889–891PubMedCrossRefGoogle Scholar
  33. Troje NF, Frost BJ (2000) Head-bobbing in pigeons: how stable is the hold phase. J Exp Bio 203:935–940Google Scholar
  34. Tweed D, Cadera W, Vilis T (1990) Computing three-dimensional eye position quaternions and eye velocity from search coil signals. Vision Res 30:97–110PubMedCrossRefGoogle Scholar
  35. Wagner H (1982) Flow-field variables trigger landing in flies. Nature 297:147–148CrossRefGoogle Scholar
  36. Wagner H (1989) Peering in barn owls. In: Erber J, Menzel R, Pflüger HJ, Todt DG (eds) Neural mechanisms of behavior. Thieme Verlag, New York, pp 238–239Google Scholar
  37. Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl’s space map. J Neurosci 13:371–386PubMedGoogle Scholar
  38. Wallach H, O’Connel DN (1953) The kinetic depth effect. J Exp Psychol 45:205–217PubMedCrossRefGoogle Scholar
  39. van der Willigen RF, Frost BJ, Wagner H (2002) Depth generalization from stereo to motion parallax in the owl. J Comp Physiol A 187:997–1007CrossRefGoogle Scholar
  40. Zeil J (1993) Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera): I. description of flight. J Comp Physiol A 172:189–205CrossRefGoogle Scholar
  41. Zhang Z (2000) A flexible new technique for camera calibration. IEEE Trans Pattern Anal Mach Intell 22:1330–1334CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Shay Ohayon
    • 1
  • Robert F. van der Willigen
    • 1
  • Hermann Wagner
    • 1
  • Igor Katsman
    • 2
  • Ehud Rivlin
    • 2
  1. 1.Institute of Biology IIRWTH UniversityAachenGermany
  2. 2.Computer Science DepartmentIsrael Institute of Technology, TechnionHaifaIsrael

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