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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

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Abstract

We investigated gaze-stabilizing reflexes in the chameleon using the three-dimensional search-coil technique. Animals were rotated sinusoidally around an earth-vertical axis under head-fixed and head-free conditions, in the dark and in the light. Gain, phase and the influence of eye position on vestibulo-ocular reflex rotation axes were studied. During head-restrained stimulation in the dark, vestibulo-ocular reflex gaze gains were low (0.1–0.3) and phase lead decreased with increasing frequencies (from 100° at 0.04 Hz to <30° at 1 Hz). Gaze gains were larger during stimulation in the light (0.1–0.8) with a smaller phase lead (<30°) and were close to unity during the head-free conditions (around 0.6 in the dark, around 0.8 in the light) with small phase leads. These results confirm earlier findings that chameleons have a low vestibulo-ocular reflex gain during head-fixed conditions and stimulation in the dark and higher gains during head-free stimulation in the light. Vestibulo-ocular reflex eye rotation axes were roughly aligned with the head's rotation axis and did not systematically tilt when the animals were looking eccentrically, up- or downward (as predicted by Listing's Law). Therefore, vestibulo-ocular reflex responses in the chameleon follow a strategy, which optimally stabilizes the entire retinal images, a result previously found in non-human primates.

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Abbreviations

2D:

two dimensional

3D:

three dimensional

LED:

light emitting diode

LL:

Listing's Law

OCR:

opto-collic reflex

OKR:

opto-kinetic reflex

VCR:

vestibulo-collic reflex

VOR:

vestibulo-ocular reflex

VP:

velocity plane

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Acknowledgements

H.H. would like to express her gratitude to Volker Henn, who initiated this project a few months before he died. Many thanks to Jan Cabungcal, Hansjörg Scherberger, Simon Elsaesser and Bernhard Hess. We would like to thank Paul Hofman, University of Nijmegen, for his permission to use his desaccading program Megadet. Animal housing and experiments were carried out in accordance with the regulations of the Veterinary Office of the Canton of Zurich, the European Communities Council Directive of 24 November 1986 (86/609/EEC), and guidelines of the Animal Welfare Committee of the University Hospital of Zürich.

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Correspondence to H. Haker.

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Volker Henn died on 3 December 1997

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Haker, H., Misslisch, H., Ott, M. et al. 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, 509–517 (2003). https://doi.org/10.1007/s00359-003-0426-y

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