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Independent eye movements in the turtle

Published online by Cambridge University Press:  02 June 2009

M. Ariel
Affiliation:
Departments of Behavioral Neuroscience and Psychiatry, University of Pittsburgh and its Center for Neuroscience, Pittsburgh

Abstract

In order to evaluate the normal eye movements of the turtle, Pseudemys scripta elegans, the positions of each eye were recorded simultaneously using two search-coil contact lenses. Optokinetic nystagmus (OKN) was strikingly unyoked in this animal such that one eye's slow-phase velocity was substantially independent of that of the other eye. On the other hand, the fast-phase motions of both eyes occurred more or less in synchrony.

An eye's slow-phase gain is primarily dependent on the direction and velocity of the stimulus to that eye. Using monocular stimuli, the highest mean gain (0.54 ± 0.047; mean ± standard error of mean) occurred using temporal-to-nasal movement at 2.5 deg/s. The mean OKN gain for nasal-to-temporal movement was only 0.13 ± 0.015 at that velocity. Additionally, using the optimal monocular stimulus (temporal-to-nasal stimulation at 2.5 deg/s) only drove the occluded eye to move nasal-to-temporally at 0.085 deg/s, equivalent to a “gain” of only 0.034 ± 0.011.

The binocular OKN gain during rotational stimuli was higher than monocular gain, especially during nasal-to-temporal movement at high velocities. Also the difference in slow-phase eye velocity between the two eyes was smaller during binocular rotational stimuli. In contrast, when each eye simultaneously viewed its temporal-to-nasal stimulus at an equal velocity, two behaviors were observed. Often, OKN alternated between an animal's left eye and right eye. Occasionally, both eyes moved at equal but opposite velocities.

These behavioral data provide a quantitative baseline to interpret the properties of the retinal slip information in the turtle's accessory optic system. Those properties are similar to the behavior of the turtle in that both are tuned to direction and velocity independently for each eye (Rosenberg & Ariel, 1990).

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

Ariel, M. (1989). Analysis of vertebrate eye movements following intravitreal drug injections, III: Spontaneous nystagmus is modulated by the GABAa receptor. Journal of Neurophysiology 62, 469480.CrossRefGoogle ScholarPubMed
Ariel, M. (1990). Analysis of vertebrate eye movements following intravitreal drug injections, V: Drug-induced eye movements are unyoked in the turtle. Journal of Neurophysiology (in press).Google Scholar
Ariel, M. & Adolph, A.R. (1985). Synaptic pharmacology of directionally sensitive ganglion cells in turtle retina. Journal of Neurophysiology 54, 123143.CrossRefGoogle Scholar
Ariel, M., Robinson, F.R. & Knapp, A.G. (1988). Analysis of vertebrate eye movements following intravitreal drug injections, II: Spontaneous nystagmus induced by picrotoxin is mediated subcortically. Journal of Neurophysiology 60, 10221035.CrossRefGoogle ScholarPubMed
Bass, A.H. & Northcutt, R.G. (1981). Retinal recipient nuclei in the painted turtle, Chrysemys picta: an autoradiographic and HRP study. Journal of Comparative Neurology 199, 97112.CrossRefGoogle ScholarPubMed
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology 299, 173196.CrossRefGoogle ScholarPubMed
Collewijn, H., Erkelens, C.J. & Steinman, R.M. (1988). Binocular coordination of human horizontal saccadic eye movements. Journal of Physiology 404, 157182.CrossRefGoogle ScholarPubMed
Collewijn, H. & Noorduin, H. (1972). Conjugate and disconjunctive optokinetic eye movements in the rabbit evoked by rotatory and translatory movements. European Journal of Physiology 335, 173185.CrossRefGoogle Scholar
Dieringer, N., Cochran, S.L. & Precht, W. (1983). Differences in the central organization of gaze stabilizing reflexes between frog and turtle. Journal of Comparative Physiology 153, 495508.CrossRefGoogle Scholar
Erkelens, C.J., Collewijn, H. & Steinman, R.M. (1989). Asymmetrical adaptation of human saccades to anisometropic spectacles. Investigative Ophthalmology and Visual Sciences 30, 11321145.Google ScholarPubMed
Fite, K.V., Reiner, A. & Hunt, S.P. (1979). Optokinetic nystagmus and the accessory optic system of pigeon and turtle. Brain Behavior Evolution 16, 192202.CrossRefGoogle ScholarPubMed
Granda, A.M. & Fulbrook, J.E. (1989). Classification of turtle retinal ganglion cells. Journal of Neurophysiology 62, 723737.CrossRefGoogle ScholarPubMed
Grasse, K.L., Cynader, M.S. & Douglas, R.M. (1984). Alterations in response properties in lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions. Experimental Brain Research 55, 6980.CrossRefGoogle ScholarPubMed
Hamada, T. (1986). Nonconjugate monocular optokinetic nystagmus in cats. Vision Research 26, 13111314.CrossRefGoogle ScholarPubMed
Kapoula, Z., Robinson, D.A. & Hain, T.C. (1986). Motion of the eye immediately after a saccade. Experimental Brain Research 61, 386394.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions in Biomedical Engineering 10, 137145.Google ScholarPubMed
Rosenberg, A.F. & Ariel, M. (1990). Visual response properties of the turtle's basal optic nucleus in vitro, Journal of Neurophysiology 63, 10331045.CrossRefGoogle ScholarPubMed
Schor, C.M., Gleason, G. & Homer, D.G. (1988). The variability and adaptability of Hering's Law for yoked reflexive eye movements. Investigative Ophthalmology and Visual Sciences (Suppl.) 29, 136.Google Scholar
Schuerger, R.J., Rosenberg, A.F. & Ariel, M. (1990). Retinal direction-sensitive input to the accessory optic system: an in vitro approach with behavioral relevance. Brain Research (in press).CrossRefGoogle Scholar
Shimazu, H. & Precht, W. (1966). Inhibition of the central vestibular neurons from the contralateral labyrinth and its mediating pathway. Journal of Neurophysiology 29, 467492.CrossRefGoogle ScholarPubMed
Steinman, R.M. & Collewijn, H. (1980). Binocular retinal-image motion during active head rotation. Vision Research 20, 415429.CrossRefGoogle ScholarPubMed
Ter Braak, J.W.G. (1936). Untersuchungen über optokinetischen nystagmus. Archives of Physiology (Netherlands) 21, 309376.Google Scholar
Wood, C.C., Spear, P.D. & Brown, J.J. (1973). Direction-specific deficits in horizontal optokinetic nystagmus following removal of visual cortex in the cat. Brain Research 60, 231237.CrossRefGoogle ScholarPubMed
Woodbury, P.B. & Ulinski, P.S. (1986). Conduction velocity, size, and distribution of optic nerve axons in the turtle, Pseudemys scripta elegans. Anatomy and Embryology 174, 253263.CrossRefGoogle ScholarPubMed