Experimental Brain Research

, Volume 223, Issue 2, pp 233–249 | Cite as

Mind the step: complementary effects of an implicit task on eye and head movements in real-life gaze allocation

  • Bernard Marius ’t HartEmail author
  • Wolfgang Einhäuser
Research Article


Gaze in real-world scenarios is controlled by a huge variety of parameters, such as stimulus features, instructions or context, all of which have been studied systematically in laboratory studies. It is, however, unclear how these results transfer to real-world situations, when participants are largely unconstrained in their behavior. Here we measure eye and head orientation and gaze in two conditions, in which we ask participants to negotiate paths in a real-world outdoor environment. The implicit task set is varied by using paths of different irregularity: In one condition, the path consists of irregularly placed steps, and in the other condition, a cobbled road is used. With both paths located adjacently, the visual environment (i.e., context and features) for both conditions is virtually identical, as is the instruction. We show that terrain regularity causes differences in head orientation and gaze behavior, specifically in the vertical direction. Participants direct head and eyes lower when terrain irregularity increases. While head orientation is not affected otherwise, vertical spread of eye-in-head orientation also increases significantly for more irregular terrain. This is accompanied by altered patterns of eye movements, which compensate for the lower average gaze to still inspect the visual environment. Our results quantify the importance of implicit task demands for gaze allocation in the real world, and imply qualitatively distinct contributions of eyes and head in gaze allocation. This underlines the care that needs to be taken when inferring real-world behavior from constrained laboratory data.


Gaze Eye movements Head orientation Natural environment Terrain negotiation Visuomotor routines 



This research was supported by the Deutsche Forschungs Gemeinschaft (German Research Foundation) research training group DFG 885/1 to BMtH and DFG grant EI 852/1 to WE. We thank Josef Stoll for his assistance and Ben Tatler for feedback on an earlier version of the manuscript.


  1. Ballard DH, Hayhoe MM (2009) Modelling the role of task in the control of gaze. Vis Cogn 17(6–7):1185–1204PubMedCrossRefGoogle Scholar
  2. Bardy BG, Warren WH, Kay BA (1996) Motion parallax is used to control postural sway during walking. Exp Brain Res 111:271–282PubMedCrossRefGoogle Scholar
  3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57(1):289–300Google Scholar
  4. Bouguet J-Y (2010) Camera Calibration Toolbox for Matlab. URL: Downloaded 13th Dec 2010
  5. Buswell GT (1935) How people look at pictures: a study of the psychology of perception in art. University of Chicago Press, ChicagoGoogle Scholar
  6. Calow D, Lappe M (2008) Efficient encoding of natural optic flow. Netw Comput Neural Syst 19(3):183–212CrossRefGoogle Scholar
  7. Castelhano MS, Mack ML, Henderson JM (2009) Viewing task influences eye movement control during active scene perception. J Vis 9(3):6.1–615CrossRefGoogle Scholar
  8. Cavanagh PR, Higginson JS (2002) What is the role of vision during stair descent? In: Andre J, Owens DA, Harvey LO (eds) Visual perception: the influence of H W Leibowitz. American Psychological Association, Washington, DC, pp 213–230Google Scholar
  9. Chapman GJ, Hollands MA (2006a) Age-related differences in stepping performance during step cycle-related removal of vision. Exp Brain Res 174:613–621PubMedCrossRefGoogle Scholar
  10. Chapman GJ, Hollands MA (2006b) Evidence for a link between changes to gaze behaviour and risk of falling in older adults during locomotion. Gait Posture 24(3):288–294PubMedCrossRefGoogle Scholar
  11. Corin MS, Elizan TS, Bender MB (1972) Oculomotor function in patients with Parkinson’s disease. J Neurol Sci 15:251–265PubMedCrossRefGoogle Scholar
  12. Cristino F, Baddeley R (2009) The nature of the visual representations involved in eye movements when walking down the street. Vis Cogn 17(6/7):880–903CrossRefGoogle Scholar
  13. DiFabio RP, Zampieri C, Greany JF (2003) Aging and saccade-stepping interactions in humans. Neurosci Lett 339(3):179–182CrossRefGoogle Scholar
  14. Droll JA, Eckstein MP (2009) Gaze control and memory for objects while walking in a real world environment. Vis Cogn 17(6/7):1159–1184CrossRefGoogle Scholar
  15. Ehinger KA, Hidalgo-Sotelo B, Torralba A, Oliva A (2009) Modelling search for people in 900 scenes: a combined source model of eye guidance. Vis Cogn 17(6/7):945–978PubMedCrossRefGoogle Scholar
  16. Einhäuser W, Rutishauser U, Koch C (2008) Task-demands can immediately reverse the effect of sensory-driven saliency in complex visual stimuli. J Vis 8(2):2.1–219CrossRefGoogle Scholar
  17. Fitzpatrick RC, Wardman DL, Taylor JL (1999) Effects of galvanic vestibular stimulation during human walking. J Physiol 517(3):931–939PubMedCrossRefGoogle Scholar
  18. Foulsham M, Walker E, Kingstone A (2011) The where, what and when of gaze allocation in the lab and the natural environment. Vis Res 51(17):1920–1931PubMedCrossRefGoogle Scholar
  19. Geruschat DR, Hassan SE, Turano K (2003) Gaze behavior while crossing complex intersections. Optom Vis Sci 80(7):515–528PubMedCrossRefGoogle Scholar
  20. Guitton D, Volle M (1987) Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58(3):427–459PubMedGoogle Scholar
  21. Hannus A, Cornelissen FW, Lindemann O, Bekkering H (2005) Selection-for-action in visual search. Acta Psychol (Amst) 118(1–2):171–191CrossRefGoogle Scholar
  22. ’t Hart BM, Vockeroth J, Schumann F, Bartl K, Schneider E, König P, Einhäuser W (2009) Gaze allocation in natural stimuli: comparing free exploration to head-fixed viewing conditions. Vis Cogn 17(6/7):1132–1158CrossRefGoogle Scholar
  23. Hausdorff JM, Yogev G, Springer S, Simon ES, Giladi N (2005) Walking is more like catching than tapping: gait in the elderly as a complex cognitive task. Exp Brain Res 164:541–548PubMedCrossRefGoogle Scholar
  24. Hayhoe M, Ballard D (2005) Eye movements in natural behavior. Trends Cogn Sci 9(4):188–194PubMedCrossRefGoogle Scholar
  25. Hayhoe M, Mennie N, Sullivan B, Gorgos K (2005) The role of internal models and prediction in catching balls Proc Conf AAAI Artif Intell 2005 Fall SymposiumGoogle Scholar
  26. Hayhoe M, Gillam B, Chajka K, Vecellio E (2009) The role of binocular vision in walking. Vis Neurosci 26:73–80PubMedCrossRefGoogle Scholar
  27. Henderson JM, Brockmole JR, Castelhano MS, Mack M (2007) Visual saliency does not account for eye-movements during visual search in real-world scenes. In: Van Gompel R, Fischer M, Murray W, Hills R (eds) Eye movement research: insights into mind and brain. Elsevier, Oxford, pp 437–562Google Scholar
  28. Hollands MA, Marple-Horvat DE (1996) Visually guided stepping under conditions of step cycle-related denial of visual information. Exp Brain Res 109:343–356PubMedCrossRefGoogle Scholar
  29. Hollands MA, Ziavra NV, Bronstein AM (2004) A new paradigm to investigate the role of head and eye movements in the coordination of whole-body movements. Exp Brain Res 154:261–266PubMedCrossRefGoogle Scholar
  30. Imai T, Moore ST, Raphan T, Cohen B (2001) Interaction of the body, head, and eyes during walking and turning. Exp Brain Res 136:1–18PubMedCrossRefGoogle Scholar
  31. Itti L, Koch C (2000) A saliency-based search mechanism for overt and covert shifts of visual attention. Vision Res 40:1489–1506PubMedCrossRefGoogle Scholar
  32. Jahn K, Strupp M, Schneider E, Dieterich M, Brandt T (2000) Differential effects of vestibular stimulation on walking and running. Neuro Rep 11(8):1745–1748Google Scholar
  33. Jahn K, Zwergal A, Schniepp R (2010) Gait disturbances in old age. Dtsch Arztebl Int 107(17):306–316PubMedGoogle Scholar
  34. Jovancevic-Misic J, Hayhoe M (2009) Adaptive gaze control in natural environments. J Neurosci 29(19):6234–6238PubMedCrossRefGoogle Scholar
  35. Kandil FI, Rotter A, Lappe M (2009) Driving is smoother and more stable when using the tangent point. J Vis 9(1):11.1–1111CrossRefGoogle Scholar
  36. Land MF (1992) Predicting eye-head coordination during driving. Nature 359(6393):318–320PubMedCrossRefGoogle Scholar
  37. Land MF (2004) The coordination of rotations of the eyes, head and trunk in saccadic turns produced in natural situations. Exp Brain Res 159:151–160PubMedCrossRefGoogle Scholar
  38. Land MF, McLeod P (2000) From eye movements to actions: how batsmen hit the ball. Nat Neurosci 3:1340–1345PubMedCrossRefGoogle Scholar
  39. Land MF, Tatler BW (2001) Steering with the head: the visual strategy of a racing driver. Curr Biol 11:1215–1220PubMedCrossRefGoogle Scholar
  40. Land M, Mennie N, Rusted J (1999) The role of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328PubMedCrossRefGoogle Scholar
  41. Marigold DS, Patla AE (2007) Gaze fixation patterns for negotiating complex ground terrain. Neuroscience 144:302–313PubMedCrossRefGoogle Scholar
  42. Marigold DS, Patla AE (2008) Visual information from the lower visual field is important for walking across multi-surface terrain. Exp Brain Res 188(1):23–31PubMedCrossRefGoogle Scholar
  43. Marx S, Respondek G, Stamelou M, Dowiasch S, Stoll J, Bremmer F, Oertel WH, Höglinger GU, Einhäuser W (in press) Validation of mobile eye tracking as novel and efficient means for differentiating progressive supranuclear palsy from Parkinson’s disease. Mov DisordGoogle Scholar
  44. Patla AE, Vickers JN (2003) How far ahead do we look when required to step on specific locations in the travel during locomotion? Exp Brain Res 148:133–138PubMedCrossRefGoogle Scholar
  45. Pelz JB, Rothkopf C (2007) Oculomotor behavior in natural and man-made environments. In: Van Gompel RPG, Fischer MH, Murray WS, Hill RL (eds) Eye Movements: A Window on Mind and Brain. Elsevier, AmsterdamGoogle Scholar
  46. Pinkhardt EH, Jürgens R, Becker W, Valdarno F, Ludolph AC, Kassubek J (2008) Differential diagnostic value of eye movement recording in PSP-parkinsonism, Richardsons’s syndrome, and idiopathic Parkinson’s disease. J Neurol 255(12):1432–1459CrossRefGoogle Scholar
  47. Rothkopf CA, Ballard DH (2009) Image statistics at the point of gaze during human navigation. Vis Neurosci 26:81–92PubMedCrossRefGoogle Scholar
  48. Schneider E, Villgrattner T, Vockeroth J, Bartl K, Kohlbecher S, Bardins S, Ulbrich H, Brandt T (2009) EyeSeeCam: an eye movement-driven head camera for the examination of natural visual exploration. Ann N Y Acad Sci 1164:461–467PubMedCrossRefGoogle Scholar
  49. Schumann F, Einhäuser W, Vockeroth J, Bartl K, Schneider E, König P (2008) Salient features in gaze-aligned recordings of human visual input during free exploration of natural environments. J Vis 8(14):12.1–1217CrossRefGoogle Scholar
  50. Smeets JBJ, Hayhoe MM, Ballard DH (1996) Goal-directed arm movements change eye-head coordination. Exp Brain Res 109(3):434–440PubMedCrossRefGoogle Scholar
  51. Startzell JK, Owens DA, Mulfinger LM, Cavanagh PR (2000) Stair negotiating in older people: a review. J Am Geriatr Soc 48:567–580PubMedGoogle Scholar
  52. Tatler BW (2007) The central fixation bias in scene viewing: selecting an optimal viewing position independently of motor biases and image feature distributions J Vis 7(14):4.1–417Google Scholar
  53. Timmis MA, Bennett SJ, Buckley JG (2009) Visuomotor control of step descent: evidence of specialised role of the lower visual field. Exp Brain Res 195:219–227PubMedCrossRefGoogle Scholar
  54. Torralba A (2003) Contextual priming for object detection. Int J Comput Vis 53(2):169–191CrossRefGoogle Scholar
  55. Treisman A, Gelade G (1980) A feature integration theory of attention. Cogn Psychol 12:97–136PubMedCrossRefGoogle Scholar
  56. Triesch J, Ballard DH, Hayhoe MM, Sullivan BT (2003) What you see is what you need. J Vis 3(1):9.86–9.94CrossRefGoogle Scholar
  57. van Koningsbruggen MG, Pender T, Machado L, Rafal RD (2009) Impaired control of the oculomotor reflexes in Parkinson’s disease. Neuropsychologia 47:2909–2915PubMedCrossRefGoogle Scholar
  58. Võ ML, Henderson JM (2011) Object-scene inconsistencies do not capture gaze: evidence from the flash-preview moving-window paradigm. Atten Percept Psychophys 73(6):1742–1753PubMedCrossRefGoogle Scholar
  59. Warren WH Jr, Kay BA, Zosh WD, Duchon AP, Sahuc S (2001) Optic flow is used to control human walking. Nat Neurosci 4(2):213–216PubMedCrossRefGoogle Scholar
  60. Wolfe JM (2007) Guided Search 4.0: Current Progress with a model of visual search. In: Gray W (ed) Integrated models of cognitive systems. New York, Oxford, pp 99–119CrossRefGoogle Scholar
  61. Wolfe JM, Cave KR, Franzel SL (1989) Guided search: an alternative to the feature integration model for visual search. J Exp Psychol Hum Percept Perform 15(3):419–433PubMedCrossRefGoogle Scholar
  62. Yarbus AL (1967) Eye movements and vision. Plenum Press, New YorkGoogle Scholar
  63. Zampieri C, Di Fabio RP (2008) Balance and eye movement training to improve gait in people with progressive supranuclear palsy: quasi-randomized clinical trial. Phys Ther 88(12):1460–1473PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Bernard Marius ’t Hart
    • 1
    Email author
  • Wolfgang Einhäuser
    • 1
  1. 1.NeurophysicsPhilipps-University MarburgMarburgGermany

Personalised recommendations