Abstract
Horizontal movements of both eyes were recorded simultaneously using scleral search coils in 2 rhesus monkeys before and after the COSMOS 2229 spaceflight of 1992–1993. Another 9 monkeys were tested at comparable time intervals and served as controls. Ocular vergence, defined as the difference in horizontal position between the left and right eyes, was measured during off-vertical yaw axis rotation (OVAR) in darkness. Vergence was modulated sinusoidally as a function of head position with regard to gravity during OVAR. The amplitude of peak-to-peak modulation increased with increments in tilt of the angle of the rotational axis (OVAR tilt angle) that ranged from 15° to 90°. Of the 11 monkeys tested, 1 had no measurable modulation in vergence. In the other 10, the mean amplitude of the peak to peak modulation was 5.5°±1.3° at 90° tilt. Each of these monkeys had maximal vergence when its nose was pointed close to upward (gravity back; mean phase: -0.9°±26°). After space flight, the modulation in vergence was reduced by over 50% for the two flight monkeys, but the phase of vergence modulation was not altered. The reduction in vergence modulation was sustained for the 11-day postflight testing period. We conclude that changes in vergence are induced in monkeys by the sinusoidal component of gravity acting along the naso-occipital axis during yaw axis OVAR, and that the modulation of the vergence reflex is significantly less sensitive to linear acceleration after space flight.
Similar content being viewed by others
References
Benson AJ, Bodin MA (1966) Interaction of linear and angular acceleration on vestibular receptors in man. Aerospace Med 37:144–154
Büttner-Ennever JA (1992) Patterns of connectivity in the vestibular nuclei. Sensing and controlling motion. Ann NY Acad Sci 656:363–378
Clendaniel RA, Mays LE (1994) Characteristics of antidromically identified oculomotor internuclear neurons during vergence and versional eye movements. J Neurophysiol 71:1111–1127
Cohen B, Suzuki J, Raphan T (1983) Role of the otolith organs in generation of horizontal nystagmus: effects of selective labyrinthine lesions Brain Res 276:159–164
Cohen B, Kozlovskaya I, Raphan T, Solomon D, Helwig D, Cohen N, Sirota M, Yakushin S (1992) Vestibular reflex of rhesus monkeys after spaceflight. J Appl Physiol Suppl 73:121–31
Correia MJ, Guedry FE (1966) Modification of vestibular response as a function of rotation about an earth-horizontal axis. Acta Otolaryngol (Stockh) 62:297–308
Correia MJ, Money KJ (1970) The effect of blockage of all six semicircular canal ducts on nystagmus produced by linear acceleration in the cat. Acta Otolaryngol (Stockh) 69:7–16
Dai MJ,McGarvie L, Kozlovskaya I, Raphan T, Cohen B (1994) Effects of space flight on ocular counterrolling and the spatial orientation of the vestibular system. Exp Brain Res 102:45–56
Darlot C, Denies P, Droulez B, Cohen B, Berthoz A (1988) Eye movements induced by off-vertical axis rotation (OVAR) at small angle of tilt. Exp Brain Res 73:91–105
Fernandez C, Goldberg J (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long duration cetrifugal force. J Neurophysiol 39:970–984
Guedry FE (1965) Orientation of the rotation axis relative to the gravity: its influence on nystagmus and the sense of rotation. Acta Otolaryngol (Stockh) 60:30–48
Hess B, Angelaki D (1993) Otolith contribution to gaze stabilization. In: Berthoz A (ed) Multisensory control of movement. Oxford Scientific, Oxford, pp 51–72
Hess BJM, Dieringer N (1990) Spatial organization of the maculoocular reflex of the rat: Response during off-vertical axis rotation. Eur J Neurosci 2:909–919
Hess BJM, Dieringer N (1991) Spatial organization of linear vestibuloocular reflex of the rat: responses during horizontal and vertical acceleration. J Neurophysiol 66:1805–1818
Hess BJM, Haslwanter TH (1991) Conjugate and non-conjugate 3D eye movements during static and dynamic otolith stimulation in the monkey. Soc Neurosci Abs 17:138
Heuer H, Dunkel-Abels G, Brüwer M, Kroger, Römer T, Wischmeier E (1988) The effects of sustained vertical gaze deviation on the resting state of the vergence system. Vision Res 28:1337–44
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
Kasper J, Shor RH, Wilson VJ (1989) Neck-vestibular interaction in the vestibular nuclei. Acta Otolaryngol Suppl (Stockh) 468:137–139
Mayne R (1974) A systems concept of the vestibular organs. In: Kornhuber HH (ed) Handbook of vestibular physiology: vestibular system. Springer, New York Berlin Heidelberg, pp 493–580
Niven JI, Hixson WC, et al (1966) Elicitation of horizontal nystagmus by periodic linear acceleration. Acta Otolaryngol (Stockh) 62:429–441
Page GD (1996) How does the linear vestibulo-ocular reflex compare with the angular vestibulo-ocular reflex? In: Baloh RW, Halmagyi GM (eds). Disorders of the vestibular system. Oxford University Press, New York, pp 93–104
Paige GD, Tomko, DL (1991) Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 65:1183–1196
Paige GD, Barnes GR, Telford L, Seidman SH (1996) Influence of sensori-motor context on the linear vestibulo-ocular reflex. Ann NY Acad Sci (in press)
Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248
Raphan T, Cohen B, Kenn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann NY Acad Sci 374:44–55
Reisine H, Highstein SM (1979) The ascending tract of Deiters' conveys a head velocity signal to medial rectus motoneurons. Brain Res 170:172–176
Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res 92:209–226
Reisine H, Strassman A, Highstein SM (1981) Eye position and head velocity signal are conveyed to medial rectus motoneuron in the alert cat by ascending tract of Deiters'. Brain Res 211:153–157
Ross MD (1993) Morphological changes in rat vestibular system following weightlessnes. J Vestib Res 3:241–251
Ross MD (1994) A spaceflight study of synaptic plasticity in adult rat vestibular maculas. Acta Otolaryngol Suppl (Stockh) 516:1–14
Schor RH, Miller AD Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. 1. Direction of maximum sensitivity. J Neurophysiol 51:136–146
Smith R (1985) Vergence eye-movement response to whole-body linear acceleration stimuli in man. Ophthalmic Physiol Opt 5:303–311
Tomko DL, Kozlovskaya IB, Paige GD, Badakva AM (1993) Adaptation to micro-gravity of oculomotor reflexes (AMOR): otolith-ocular reflexes. (Final science report) NASA, NASA-Ames Research Center, Mountainview, CA
Van Opstal AJ, Hepp K, Suzuki Y, Henn V (1995) Influence of eye position on activity in monkey superior colliculus. J Neurophysiol 74:1593–1610
Yakushin S, Dai M, Suzuki J, Raphan T, Cohen B (1995) Semicircular canal contributions to the three-dimensional vestibuloocular reflex: a model-based approach. J Neurophysiol 74:2722–2738
Young LR, Henn V (1975) Nystagmus produced by pitch and yaw rotation of monkeys. Fortschr Zool 23:235–246
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Dai, M., Raphan, T., Kozlovskaya, I. et al. Modulation of vergence by off-vertical yaw axis rotation in the monkey normal characteristics and effects of space flight. Exp Brain Res 111, 21–29 (1996). https://doi.org/10.1007/BF00229551
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00229551