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Head–eye interactions during vertical gaze shifts made by rhesus monkeys

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Abstract

Changing the direction of the line of sight (gaze) can involve coordinated movements of the eyes and head. During gaze shifts directed along the horizontal meridian, the contribution of the eyes and head depends upon the position of the eyes in the orbits; the contribution of the head to accomplishing the overall shift in gaze declines as the eyes increasingly are deviated away from the direction of the ensuing gaze shift. Also during horizontal gaze shifts, changes in the metrics and kinematics of the saccadic (eye movement) portion of coordinated movements, are correlated with the amplitude and velocity of the concurrent head movement. With increasing head contributions, saccade peak velocities decline, durations increase and velocity profiles develop two peaks. It remains unknown whether the interaction between head and eyes observed during horizontal gaze shifts also occurs during vertical gaze shifts. Yet, a full understanding of the neural control of eye–head coordination will depend upon the correlation of neural activity and features of vertical as well as horizontal movements. This report describes the metrics and kinematics of vertical gaze shifts made by head-unrestrained rhesus monkeys. Key observations include: (1) during vertical gaze shifts of a particular amplitude, relative eye and head contributions depend upon the initial vertical positions of the eyes in the orbits; (2) as head contribution increases, peak eye velocities decline, durations increase and vertical velocity profiles develop two peaks; (3) head movement metrics and kinematics are accurately predictable given knowledge only of head movement amplitude. In these ways, vertical gaze shifts were found to be qualitatively similar to horizontal gaze shifts. It seems probable that similar mechanisms mediate head–eye interactions during both horizontal and vertical movements. These observations are consistent with the hypothesis that a signal proportional to vertical head velocity reduces the gain of the vertical saccade burst generator.

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References

  • Bahill AT, Clark MR, Stark L (1975) The main sequence, a tool for studying human eye movements. Math Biosci 24:191–204

    Article  Google Scholar 

  • Baloh RW, Konrad HR, Sills AW, Honrubia V (1975) The saccade velocity test. J Neurol 25:1071–1076

    CAS  Google Scholar 

  • Becker W, Jürgens R (1990) Human oblique saccades: quantitative analysis of the relation between horizontal and vertical components. Vision Res 30:893–920

    Article  PubMed  CAS  Google Scholar 

  • Collewijn H (1977) Eye- and head movements in freely moving rabbits. J Physiol 266:471–498

    PubMed  CAS  Google Scholar 

  • Collewijn H, Erkelens CJ, Steinman RM (1988a) Binocular co-ordination of human horizontal saccadic eye movements. J Physiology 404:157–182

    CAS  Google Scholar 

  • Collewijn H, Erkelens CJ, Steinman RM (1988b) Binocular co-ordination of human vertical saccadic eye movements. J Physiol 404:183–197

    PubMed  CAS  Google Scholar 

  • Corneil BD, Olivier E, Richmond FJ, Loeb GE, Munoz DP (2001) Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. J Neurophysiol 86:1729–1749

    PubMed  CAS  Google Scholar 

  • Delreux V, Abeele SV, Lefevre P, Roucoux A (1991) Influences of eye position on the control of head movement amplitude. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 38–48

    Google Scholar 

  • Freedman EG (2001) Interactions between eye and head control signals can account for movement kinematics. Biol Cybern 84:453–462

    Article  PubMed  CAS  Google Scholar 

  • Freedman EG, Quessy S (2004) Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis II. Effects on metrics and kinematics of ongoing gaze shifts to visual targets. Exp Brain Res 156:357–376

    Article  PubMed  Google Scholar 

  • Freedman EG, Sparks DL (1997) Eye–head coordination during head-unrestrained gaze shifts in rhesus monkeys. J Neurophysiol 77:2328–2348

    PubMed  CAS  Google Scholar 

  • Freedman EG, Sparks DL (2000) Coordination of the eyes and head: movement kinematics. Exp Brain Res 131:22–32

    Article  PubMed  CAS  Google Scholar 

  • Fuller JH (1992) Head movement propensity. Exp Brain res 92:152–165

    Article  PubMed  CAS  Google Scholar 

  • Goossens HHLM, vanOpstal AJ (1997) Human eye–head coordination in two dimensions under different sensorimotor conditions. Exp Brain Res 114:542–560

    Article  PubMed  CAS  Google Scholar 

  • Guitton D, Douglas RM, Volle M (1984) Eye–head coordination in cats. J Neurophysiol 52:1030–1050

    PubMed  CAS  Google Scholar 

  • Huebner WP, Paloski WH, Reschke MF, Bloomberg JJ (1995) Geometric adjustments to account for eye eccentricity in processing horizontal and vertical eye and head movement data. J Vesitibular Res 5:299–322

    Article  CAS  Google Scholar 

  • Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535–538

    Article  PubMed  CAS  Google Scholar 

  • Phillips JO, Ling L, Fuchs AF, Seibold C, Plorde JJ (1995) Rapid horizontal gaze movement in the monkey. J Neurophysiol 73:1632–1652

    PubMed  CAS  Google Scholar 

  • Robinson DA (1964) The mechanics of human saccadic eye movement. J Physiol 174:245–264

    PubMed  CAS  Google Scholar 

  • Stahl J (1999) Amplitude of human head movements associated with horizontal saccades. Exp Brain Res 126:41–54

    Article  PubMed  CAS  Google Scholar 

  • Stahl JS (2001) Eye–head coordination and the variation of eye-movement accuracy with orbital eccentricity. Exp Brain Res 136:200–210

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson RD (1990) Combined eye–head gaze shifts in primate III. Contributions to the accuracy of gaze saccades. J Neurophysiol 64:1873–1981

    PubMed  CAS  Google Scholar 

  • Tomlinson RD, Bahra PS (1986) Combined eye–head gaze shifts in the primate I. Metrics. J Neurophysiology 56:1542–1557

    CAS  Google Scholar 

  • Tweed D, Glenn B, Vilis T (1995) Eye–head coordination during large gaze shifts. J Neurophysiol 73:766–799

    PubMed  CAS  Google Scholar 

  • Volle M, Guitton D (1993) Human gaze shifts in which the head and eyes are not initially aligned. Exp Brain Res 94:463–470

    Article  PubMed  CAS  Google Scholar 

  • Yee RD, Schiller VL, Lim V, Baloh FG, Baloh RW, Honrubia V (1985) Velocities of vertical saccades with different eye movement recording methods. Invest Ophthalmol Vis Sci 26:938–944

    PubMed  CAS  Google Scholar 

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Acknowledgements

The author thanks Dr. Gil Rivlis for development of data acquisition and behavioral control software, and G. Parker for technical assistance. This work is supported in part by NEI EY13239 and NSF IBN-0132335. Additional support provided by the Center for Visual Science (NEI P30-EY01319).

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  1. Department of Neurobiology and Anatomy, University of Rochester, Box 603, 601 Elmwood Ave., Rochester, NY, 14642, USA

    Edward G. Freedman

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  1. Edward G. Freedman
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Correspondence to Edward G. Freedman.

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Freedman, E.G. Head–eye interactions during vertical gaze shifts made by rhesus monkeys. Exp Brain Res 167, 557–570 (2005). https://doi.org/10.1007/s00221-005-0051-9

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  • DOI: https://doi.org/10.1007/s00221-005-0051-9

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