Experimental Brain Research

, Volume 191, Issue 4, pp 419–434 | Cite as

Idiosyncratic variations in eye–head coupling observed in the laboratory also manifest during spontaneous behavior in a natural setting

  • Zachary C. Thumser
  • Brian S. Oommen
  • Igor S. Kofman
  • John S. Stahl
Research Article

Abstract

The tendency to generate head movements during saccades varies from person to person. Head movement tendencies can be measured as subjects fixate sequences of illuminated targets, but the extent to which such measures reflect eye–head coupling during more natural behaviors is unknown. We quantified head movement tendencies in 20 normal subjects in a conventional laboratory experiment and in an outdoor setting in which the subjects directed their gaze spontaneously. In the laboratory, head movement tendencies during centrifugal saccades could be described by the eye-only range (EOR), customary ocular motor range (COMR), and the customary head orientation range (CHOR). An analogous EOR, COMR, and CHOR could be extracted from the centrifugal saccades executed in the outdoor setting. An additional six measures were introduced to describe the preferred ranges of eyes-in-head and head-on-torso manifest throughout the outdoor recording, i.e., not limited to the orientations following centrifugal saccades. These 12 measured variables could be distilled by factor analysis to one indoor and six outdoor factors. The factors reflect separable tendencies related to preferred ranges of visual search, head eccentricity, and eye eccentricity. Multiple correlations were found between the indoor and outdoor factors. The results demonstrate that there are multiple types of head movement tendencies, but some of these influence behavior across rather different experimental settings and tasks. Thus behavior in the two settings likely relies on common neural mechanisms, and the laboratory assays of head movement tendencies succeed in probing the mechanisms underlying eye–head coupling during more natural behaviors.

Keywords

Saccade Video oculography Eye–head coordination Gaze saccade Eye–head saccade Head-mover Human 

References

  1. Afanador A, Aitsebaono P (1982) The range of eye movements through progressive lenses. Optom Mon 73:127–135Google Scholar
  2. Bard C, Fleury M, Paillard J (1992) Different patterns in aiming accuracy for head-movers and non-head movers. In: Berthoz A, Vidal PP, Graf W (eds) The head–neck sensory motor system. Oxford University Press, New York, pp 582–586Google Scholar
  3. Chatterjee S, Price B (1977) Regression analysis by example. Wiley, New YorkGoogle Scholar
  4. Cliff N (1987) Analyzing multivariate data. Harcourt Brace Jovanovich, New YorkGoogle Scholar
  5. Draper NR, Smith H (1981) Applied regression analysis. Wiley, New YorkGoogle Scholar
  6. Einhäuser W, Schumann F, Bardins S, Bartl K, Böning G, Schneider E, König P (2007) Human eye–head co-ordination in natural exploration. Network 18:267–297PubMedCrossRefGoogle Scholar
  7. Fuller JH (1992) Head movement propensity. Exp Brain Res 92:152–164PubMedCrossRefGoogle Scholar
  8. Fuller JH (1996) Comparison of horizontal head movements evoked by auditory and visual targets. J Vestib Res 6:1–13PubMedCrossRefGoogle Scholar
  9. Geruschat DR, Hassan SE, Turano KA (2003) Gaze behavior while crossing complex intersections. Optom Vis Sci 80:515–528PubMedCrossRefGoogle Scholar
  10. Goldring JE, Dorris MC, Corneil BD, Ballantyne PA, Munoz DP (1996) Combined eye–head gaze shifts to visual and auditory targets in humans. Exp Brain Res 111:68–78PubMedCrossRefGoogle Scholar
  11. Goossens H, Van Opstal A (1997) Human eye–head coordination in two dimensions under different sensorimotor conditions. Exp Brain Res 114:542–560PubMedCrossRefGoogle Scholar
  12. Hanes DA, McCollum G (2006) Variables contributing to the coordination of rapid eye/head gaze shifts. Biol Cybern 94:300–324PubMedCrossRefGoogle Scholar
  13. Herst AN, Epelboim J, Steinman RM (2001) Temporal coordination of the human head and eye during a natural sequential tapping task. Vision Res 41:3307–3319PubMedCrossRefGoogle Scholar
  14. Hollands M, Patla A, Vickers J (2002) “Look where you’re going!”: gaze behaviour associated with maintaining and changing the direction of locomotion. Exp Brain Res 143:221–230PubMedCrossRefGoogle Scholar
  15. Kowler E, Pizlo Z, Zhu G, Erkelens CJ, Steinman RM, Collewijn H (1992) Coordination of head and eyes during the performance of natural (and unnatural) visual tasks. In: Berthoz A, Graf W, Vidal PP (eds) The head–neck sensory motor system. Oxford University Press, OxfordGoogle Scholar
  16. Land MF (1992) Predictable eye–head coordination during driving. Nature 359:318–320PubMedCrossRefGoogle Scholar
  17. Land M, Tatler B (2001) Steering with the head. the visual strategy of a racing driver. Curr Biol 11:1215–1220PubMedCrossRefGoogle Scholar
  18. Lee C (1999) Eye and head coordination in reading: roles of head movement and cognitive control. Vision Res 39:3761–3768PubMedCrossRefGoogle Scholar
  19. Oommen BS, Stahl JS (2005a) Amplitudes of head movements during putative eye-only saccades. Brain Res 1065:68–78PubMedCrossRefGoogle Scholar
  20. Oommen BS, Stahl JS (2005b) Inhibited head movements: a risk of combining phoning with other activities? Neurology 65:754–756PubMedCrossRefGoogle Scholar
  21. Oommen BS, Stahl JS (2005c) Overlapping gaze shifts reveal timing of an eye–head gate. Exp Brain Res 167:276–286PubMedCrossRefGoogle Scholar
  22. Oommen BS, Smith RM, Stahl JS (2004) The influence of future gaze orientation upon eye–head coupling during saccades. Exp Brain Res 155:9–18PubMedCrossRefGoogle Scholar
  23. Pelz J, Hayhoe M, Loeber R (2001) The coordination of eye, head, and hand movements in a natural task. Exp Brain Res 139:266–277PubMedCrossRefGoogle Scholar
  24. Proudlock F, Shekhar H, Gottlob I (2003) Coordination of eye and head movements during reading. Invest Ophthalmol Vis Sci 44:2991–2998PubMedCrossRefGoogle Scholar
  25. Silverman BW (1986) Density estimation for statistics and data analysis. Chapman and Hall, New YorkGoogle Scholar
  26. Smeets J, Hayhoe M, Ballard D (1996) Goal-directed arm movements change eye–head coordination. Exp Brain Res 109:434–440PubMedCrossRefGoogle Scholar
  27. Stahl JS (1999) Amplitude of human head movements associated with horizontal saccades. Exp Brain Res 126:41–54PubMedCrossRefGoogle Scholar
  28. Stahl JS (2001) Adaptive plasticity of head movement propensity. Exp Brain Res 139:201–208PubMedCrossRefGoogle Scholar
  29. Thumser ZC, Stahl JS (2008) Laboratory measures of eye–head coupling predict spontaneous behavior in natural environment. Soc Neurosci Abstr 34Google Scholar
  30. Volle M, Guitton D (1993) Human gaze shifts in which head and eyes are not initially aligned. Exp Brain Res 94:463–470PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Zachary C. Thumser
    • 1
  • Brian S. Oommen
    • 1
  • Igor S. Kofman
    • 1
  • John S. Stahl
    • 1
    • 2
  1. 1.Louis Stokes Cleveland Department of Veterans Affairs Medical CenterClevelandUSA
  2. 2.Department of NeurologyCase Western Reserve UniversityClevelandUSA

Personalised recommendations