Skip to main content
SpringerLink
Log in

Through a barn owl’s eyes: interactions between scene content and visual attention

  • Original Paper
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

In this study we investigated visual attention properties of freely behaving barn owls, using a miniature wireless camera attached to their heads. The tubular eye structure of barn owls makes them ideal subjects for this research since it limits their eye movements. Video sequences recorded from the owl’s point of view capture part of the visual scene as seen by the owl. Automated analysis of video sequences revealed that during an active search task, owls repeatedly and consistently direct their gaze in a way that brings objects of interest to a specific retinal location (retinal fixation area). Using a projective model that captures the geometry between the eye and the camera, we recovered the corresponding location in the recorded images (image fixation area). Recording in various types of environments (aviary, office, outdoors) revealed significant statistical differences of low level image properties at the image fixation area compared to values extracted at random image patches. These differences are in agreement with results obtained in primates in similar studies. To investigate the role of saliency and its contribution to drawing the owl’s attention, we used a popular bottom-up computational model. Saliency values at the image fixation area were typically greater than at random patches, yet were only 20% out of the maximal saliency value, suggesting a top-down modulation of gaze control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahanger G, Little T (1996) A survey of technologies for parsing and indexing digital video. J Visual Commun Image Representation 7(1): 28–43

    Article  Google Scholar 

  • Baddeley RJ, Tatler BW (2006) High frequency edges (but not contrast) predict where we fixate: a Bayesian system identification analysis. Vis Res 46: 2824–2833

    Article  PubMed  Google Scholar 

  • Baldi P, Brunak S (2001) Bioinformatics: the machine learning approach, 2nd edn. MIT, Cambridge

    Google Scholar 

  • Betsch BY, Einhäuser W, Körding KP, König P (2004) The world from a cats perspective statistics of natural videos. J Biol Cybern 90(1): 41–50

    Article  Google Scholar 

  • Buswell GT (1935) How people look at pictures. University of Chicago Press, Chicago

    Google Scholar 

  • Dailianas A, Allen R, England P (1995) Comparisons of automatic video segmentation algorithms. In: Proceedings, SPIE photonics east’95: integration issues in large commercial media delivery systems, Philadelphia

  • 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: 131–146

    PubMed  Google Scholar 

  • Einhäuser W, König P (2006) Does luminance-contrast contribute to a saliency map for overt visual attention? Euro J Neurosci 17(5):1089–1097

    Article  Google Scholar 

  • Einhäuser W, Kruse W, Hoffmann K, König P (2006) Differences of monkey and human overt attention under natural conditions. Vis Res 46(8–9): 1194–1209

    Article  PubMed  Google Scholar 

  • Field D (1987) Relations between the statistics of natural images and the response properties of cortical cells. J Opt Soc Am A 4(12): 2379–2394

    PubMed  CAS  Google Scholar 

  • Gonzalez RC, Woods RE (2001) Digital image processing. Addison-Wesley Longman Publishing Co., Inc., Boston

    Google Scholar 

  • Hartley R, Zisserman A (2000) Multiple view geometry in computer vision. Cambridge University Press, Cambridge

    Google Scholar 

  • Hayhoe MM, Ballard DH (2005) Eye movements in natural behavior. Trends Cogn Sci 9(4): 188–194

    Article  PubMed  Google Scholar 

  • Henderson J, Hollingworth A (1999) High-level scene perception. Ann Rev Psychol 50: 243–271

    Article  CAS  Google Scholar 

  • Henderson J, Brockmole J, Castelhano M, Mack M (2007) Eye movements: a window on mind and brain. In: Visual saliency does not account for eye movements during visual search in real-world scenes. Elsevier,Oxford (in prep)

  • Itti L (2005) Quantifying the contribution of low-level saliency to human eye movements in dynamic scenes. Vis Cogn 12(6): 1093–1123

    Article  Google Scholar 

  • Itti L, Koch C, Niebur E (1998) A model of saliency-based visual attention for rapid scene analysis. IEEE Trans Pattern Anal Mach Intell 20(11): 1254–1259

    Article  Google Scholar 

  • Johnen A, Wagner H, Gaese BH (2001) Spatial attention modulates sound localization in barn owls. J Neurophysiol 85(2): 1009–1012

    PubMed  CAS  Google Scholar 

  • Kayser C, Nielsen KJ, Logothetis N (2006) Fixations in natural scenes: interaction of image structure and image content. Vis Res 46(16): 2535–2545

    Article  PubMed  Google Scholar 

  • Knudsen E, Konishi M (1979) Mechanisms of sound localization in the barn owl (tyto alba). J Comp Physiol 133: 13–21

    Article  Google Scholar 

  • 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: 1–11

    Article  Google Scholar 

  • Koch C, Ullman S (1985) Shifts in selective visual attention: towards the underlying neural circuitry. Human Neurobiol (4):219–227

    CAS  Google Scholar 

  • Krieger G, Rentschler H, Hauske G, Schill K, Zetzsche C (2000) Object and scene analysis by saccadic eye-movements: an investigation with higher-order statistics. Spatial Vis 13: 201–214

    Article  CAS  Google Scholar 

  • Land M, Hayhoe M (2001) In what ways do eye movements contribute to everyday activities? Vis Res 41(25–26):3559–3565

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Pettigrew J (2003) Orientation mosaic in barn owl’s visual wulst revealed by optical imaging: comparison with cat and monkey striate and extra-striate areas. Brain Res 961(1): 153–158

    Article  PubMed  CAS  Google Scholar 

  • Mannan S, Ruddock K, Wooding D (1996) The relationship between the locations of spatial features and those of fixations made during visual examination of briefly presented images. Spatial Vis 10(3): 165–188

    CAS  Google Scholar 

  • Marr D, Hildreth E (1980) Theory of edge detection. Proc Roy Soc Lond B207:187–217

    Article  CAS  Google Scholar 

  • Martin G (1982) An owls eye: schematic optics and visual performance in strix aluco. J Comp Physiol 145(341–349)

    Google Scholar 

  • Masino T, Knudsen EI (1990) Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn owl. Nature 345: 434–437

    Article  PubMed  CAS  Google Scholar 

  • Masino T, Knudsen EI (1993) Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. J Neurosci 13: 351–370

    PubMed  CAS  Google Scholar 

  • Navalpakkam V, Itti L (2005) Modeling the influence of task on attention. Vis Res 45(2): 205–231

    Article  PubMed  Google Scholar 

  • Nieder A (1999) Mechanisms of depth perception in the visual forebrain of the behaving barn owl. PhD thesis, Rheinisch-Westfälische Technische Hochschule Aachen, Fakultät für Mathematik, Informatik und Naturwissenschaften

  • Nieder A, Wagner H (1999) Perception and neuronal coding of subjective contours in the owl. Nat Neurosci 2: 660–663

    Article  PubMed  CAS  Google Scholar 

  • Ohayon S, van der Willigen RF, Wagner H, Katsman I, Rivlin E (2006) On the barn owls visual pre-attack behavior: I. structure of head movements and motion patterns. J Comp Physiol A Neuroethol Sensory Neural Behav Physiol 192(9): 927–940

    Article  Google Scholar 

  • Parkhurst D, Niebur E (2003) Scene content selected by active vision. Spatial Vis 16(2): 125–154

    Article  Google Scholar 

  • Parkhurst D, Law K, Niebur E (2002) Modeling the role of salience in the allocation of overt visual attention. Vis Res 42(1): 107–123

    Article  PubMed  Google Scholar 

  • Payne RS (1971) Acoustic location of prey by barn owls (tyto alba). J Exp Biol 54: 535–573

    PubMed  CAS  Google Scholar 

  • Pettigrew J, Konishi M (1976) Neurons selective for orientation and binocular disparity in the visual wulst of the barn owl. Science 193(4254): 675–678

    Article  PubMed  CAS  Google Scholar 

  • Rao R, Zelinsky G, Hayhoe M, Ballard D (2002) Eye movements in iconic visual search. Vis Res 42(11): 1447–1463

    Article  PubMed  Google Scholar 

  • Reinagel P, Zador A (1999) Natural scene statistics at the center of gaze. Network Comput Neural Syst 10: 1–10

    Article  Google Scholar 

  • Steinbach M, Money K (1973) Eye movements of the owl. Vis Res 13(1): 889–891

    Article  PubMed  CAS  Google Scholar 

  • Treisman A, Gelade G (1980) A feature integration theory of attention. Cogn Psychol 12: 97–136

    Article  CAS  PubMed  Google Scholar 

  • Tucker V (2000) The deep fovea, sideways vision and spiral flight paths in raptors. J Exp Biol 203(24): 3745–3754

    PubMed  CAS  Google Scholar 

  • Vanni-Mercier G, Pelisson D, Sakai K, Jouvet M (1994) Eye saccade dynamics during paradoxical sleep in the cat. Eur J Neurosci 6(8): 1298–1306

    Article  PubMed  CAS  Google Scholar 

  • van der Willigen RF (2000) On the perceptual identity of depth vision in the owl. PhD thesis, Rheinisch-Westfälische Technische Hochschule Aachen, Fakultät für Mathematik, Informatik und Naturwissenschaften

  • van der Willigen RF, Frost BJ, Wagner H (2001) Encoding of both vertical and horizontal disparity in random-dot stereograms by wulst neurons of awake barn owls. Visual Neurosci 18: 541–554

    Article  Google Scholar 

  • Wagner H (1993) Sound-localization deficits induced by lesions in the barn owl’s space map. J Neurosci 13(1): 371–386

    PubMed  CAS  Google Scholar 

  • Walther D, Koch C (2006) Modeling attention to salient proto-objects. Neural Netw 19: 1395–1407

    Article  PubMed  Google Scholar 

  • Wathey J, Pettigrew J (1989) Quantitative analysis of the retinal ganglion cell layer and optic nerve of the barn owl tyto alba. Brain Behav Evolut 33(5): 279–292

    CAS  Google Scholar 

  • Whitchurch EA, Takahashi TT (2006) Combined auditory and visual stimuli facilitate head saccades in the barn owl (tyto alba). J Neurophysiol 96: 730–745

    Article  PubMed  Google Scholar 

  • Yarbus A (1967) Eye movements and vision. Plenum Press, New York

    Google Scholar 

  • Zaharescu A, Rothenstein A, Tsotsos J (2004) Towards a biologically plausible active visual search model. In: ECCV Workshop on attention and performance in computer vision

  • Zhang Z (2000) A flexible new technique for camera calibration. IEEE Trans Pattern Anal Mach Intell 22(11): 1330–1334

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Israel Institute of Technology (Technion), Haifa, 32000, Israel

    Shay Ohayon & Ehud Rivlin

  2. Institute of Biology II, RWTH University, Kopernikusstrasse 16, 52074, Aachen, Germany

    Wolf Harmening & Hermann Wagner

Authors
  1. Shay Ohayon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolf Harmening
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hermann Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ehud Rivlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shay Ohayon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ohayon, S., Harmening, W., Wagner, H. et al. Through a barn owl’s eyes: interactions between scene content and visual attention. Biol Cybern 98, 115–132 (2008). https://doi.org/10.1007/s00422-007-0199-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-007-0199-4

Keywords

Search

Navigation