Saccades reduce latency and increase velocity of ocular accommodation

Horizontal vergence can be stimulated binocularly with disparity (disparity vergence) or monocularly with accommodation (accommodative vergence). The latter results from a neural cross-coupling that causes both horizontal vergence and accommodation to respond when either one is stimulated [Alpern, M., & Ellen, P. (1956). American Journal of Ophthalmology, 42, 289-303]. The velocity of disparity and accommodative vergence is enhanced when accompanied by saccades [Enright, J. T. (1984). Journal of Physiology (London) 350, 9-31; Enright, J. T. (1986). Journal of Physiology (London) 371, 69-89]. Based upon the coupling between accommodation and vergence, we predicted that accommodation should also be facilitated by saccades. An SRI Dual Purkinje Eyetracker was used to measure left and right eye position, and the accommodation of the left eye, in response to stimulation. Horizontal saccades were stimulated by targets separated by 2-6 degrees and accommodation was stimulated monocularly over a range of +/- 2 diopters (D). When saccades occurred within 0-400 ms following a monocular step stimulus to accommodation, latency of accommodation decreased and the associated accommodative-vergence response was synchronized with the saccade. Saccades also enhanced the velocity of accommodation and accommodative-vergence, and this facilitation increased with saccade amplitude. Transient vergence responses that are normally associated with saccades [Erkelens, C. J., Steinman, R. M., & Collewijn, H. (1989). Proceedings of the Royal Society of London B. Biological Sciences, 236, 441-465; Maxwell, J. S., & King, W. M. (1992). Journal of Neurophysiology, 68 (4), 1248-1260] did not affect accommodation when it was not stimulated by defocus. Because saccades and accommodation utilize separate plants and final common pathways, the synchronization of saccades and accommodation and the enhanced velocity of accommodation and accommodative-vergence must occur at more central sites. Possibilities include the superior colliculus, which represents both accommodation and saccades [Nagasaka, Y., & Ohtsuka, K., (1998). Investigative Ophthalmology AVRO supplement], vestibular nuclei which project to regions near the oculomotor nuclei [Lang, W., Buttner-Ennever, J. A., & Buttner, U. (1979). Brain Research, 177, 3-17], and interactions between omni pause neurons and near response cells of the mesencephalic reticular formation (MRF) [Mays, L. E., & Gamlin, P. D. R. (1995a). Current Opinions in Neurobiology, 5, 763-768; Mays, L. E., & Gamlin, P. D. R. (1995b). Eye movement research: Mechanisms, processes and applications. New York: Elsevier] which represent both accommodation and vergence [Judge, S. J., & Cumming, B. G. (1986). Journal of Neurophysiology, 55, 915-930; Zhang, Y., Mays, L. E., & Gamli, P. D. R. (1992). Journal of Neurophysiology, 67, 944-960].

[1]  I. Donaldson.  Control of gaze by brain stem neurons Proceedings of the symposium held in the Abbaye de Royaumont. Paris 12–15 July, 1977.Developments in Neuroscience, vol. 1.R. Baker &A. Berthoz (eds). Elsevier/North Holland Biomedical Press, Amsterdam (1977). 514 + xv pp., $59.95 , 1978, Neuroscience.

[2]  C. K. Henkel,et al.  Superior colliculus connections with the extraocular motor nuclei in the cat , 1978, The Journal of comparative neurology.

[3]  L M Optican,et al.  Saccade-vergence interactions in humans. , 1992, Journal of neurophysiology.

[4]  L E Mays,et al.  Behavior of identified Edinger-Westphal neurons during ocular accommodation. , 1994, Journal of neurophysiology.

[5]  Paul D. Gamlin,et al.  A Neural Mechanism Subserving Saccade-Vergence Interactions , 1995 .

[6]  J. T. Enright.  Changes in vergence mediated by saccades. , 1984, The Journal of physiology.

[7]  Robert W. Kentridge,et al.  Eye movement research : mechanisms, processes and applications , 1995 .

[8]  Heiner Deubel,et al.  Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades , 1995, Vision Research.

[9]  W. Cleveland.  Robust Locally Weighted Regression and Smoothing Scatterplots , 1979 .

[10]  L. Mays.  Neural control of vergence eye movements: convergence and divergence neurons in midbrain. , 1984, Journal of neurophysiology.

[11]  P. May,et al.  Morphology and distribution of serotoninergic and oculomotor internuclear neurons in the cat midbrain , 1987, The Journal of comparative neurology.

[12]  L E Mays,et al.  Neural control of vergence eye movements: neurons encoding vergence velocity. , 1986, Journal of neurophysiology.

[13]  S. Judge,et al.  Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. , 1986, Journal of neurophysiology.

[14]  Lawrence E Mays,et al.  Neuronal circuitry controlling the near response , 1995, Current Opinion in Neurobiology.

[15]  H. D. Crane,et al.  Accurate three-dimensional eyetracker. , 1978, Applied optics.

[16]  D. Ruppert.  Robust Statistics: The Approach Based on Influence Functions , 1987 .

[17]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[18]  Casper J. Erkelens,et al.  Voluntary binocular gaze-shifts in the plane of regard: Dynamics of version and vergence , 1995, Vision Research.

[19]  A Oohira,et al.  Vergence eye movements facilitated by saccades. , 1993, Japanese journal of ophthalmology.

[20]  C. Zetterström.  THE EFFECT OF PHENYLEPHRINE ON THE ACCOMMODATIVE PROCESS IN MAN , 1984, Acta ophthalmologica.

[21]  Clifton M. Schor,et al.  Isovergence surfaces: the conjugacy of vertical eye movements in tertiary positions of gaze , 1994, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[22]  B. Brown,et al.  The effect of phenylephrine hydrochloride on the resting point of accommodation. , 1983, Investigative ophthalmology & visual science.

[23]  D Wilson,et al.  A centre for accommodative vergence motor control. , 1973, Vision research.

[24]  J. C. Kotulak,et al.  Temporal variations in accommodation during steady-state conditions. , 1986, Journal of the Optical Society of America. A, Optics and image science.

[25]  Hermann M. Burian.  Oculomotor Imbalance in Binocular Vision and Fixation Disparity , 1968 .

[26]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[27]  C. Schor,et al.  Negative feedback control model of proximal convergence and accommodation , 1992, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[28]  H D Crane,et al.  Generation-V dual-Purkinje-image eyetracker. , 1985, Applied optics.

[29]  E F FINCHAM,et al.  The reciprocal actions of accommodation and convergence , 1957, The Journal of physiology.

[30]  C. Henkel,et al.  The superior colliculus control of pinna movements in the cat: Possible anatomical connections , 1978, The Journal of comparative neurology.

[31]  Y. Zhang,et al.  Characteristics of near response cells projecting to the oculomotor nucleus. , 1992, Journal of neurophysiology.

[32]  W. King,et al.  Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys. , 1992, Journal of neurophysiology.

[33]  W. Charman,et al.  EFFECTS OF 0.1% CYCLOPENTOLATE OR 10% PHENYLEPHRINE ON PUPIL DIAMETER AND ACCOMMODATION , 1986, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[34]  M. Alpern,et al.  The effect of sympathomimetic drugs upon the amplitude of accommodation. , 1959, American journal of ophthalmology.

[35]  G. Mousa,et al.  Effect of phenylephrine on accommodation. , 1986, American journal of optometry and physiological optics.

[36]  L. Stark,et al.  Unequal saccades during vergence. , 1980, American journal of optometry and physiological optics.

[37]  K. Ohtsuka,et al.  Lens accommodation evoked by micro-stimulation of the superior colliculus in the cat , 1994, Vision Research.

[38]  W. Cleveland,et al.  Locally Weighted Regression: An Approach to Regression Analysis by Local Fitting , 1988 .

[39]  K. Ohtsuka,et al.  Projection from the accommodation‐related area in the superior colliculus of the cat , 1996, The Journal of comparative neurology.

[40]  M. Sanders.  Control of Gaze by Brain Stem Neurons , 1978 .

[41]  CASPER J ERKELENS,et al.  Trajectories of the Human Binocular Fixation Point during Conjugate and Non-conjugate Gaze-shifts , 1997, Vision Research.

[42]  D L Robinson,et al.  Superior colliculus neurons studied during head and eye movements of the behaving monkey. , 1974, Journal of neurophysiology.

[43]  H Collewijn,et al.  Ocular vergence under natural conditions. II. Gaze shifts between real targets differing in distance and direction , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[44]  J. T. Enright,et al.  Facilitation of vergence changes by saccades: influences of misfocused images and of disparity stimuli in man. , 1986, The Journal of physiology.

[45]  K Ohtsuka,et al.  Divergent axon collaterals from the rostral superior colliculus to the pretectal accommodation‐related areas and the omnipause neuron area in the cat , 1999, The Journal of comparative neurology.

[46]  U. Büttner,et al.  Vestibular projections to the monkey thalamus: An autoradiographic study , 1979, Brain Research.

[47]  J. C. Kotulak,et al.  Dynamic interactions between accommodation and convergence are velocity sensitive , 1986, Vision Research.