Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Eye‐Head Coordination

Emilio Bizzi

10.1002/cphy.cp010229

Source: Supplement 2: Handbook of Physiology, The Nervous System, Motor Control

Originally published: 1981

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Eye‐Head Coordination After Appearance of Unexpected and Stationary Target in Space
1.1 Saccades During Head Movement
1.2 Compensatory Eye Movements
1.3 Head Movement
1.4 Summary and Schematic Outline of Eye‐Head Coordination
2 Eye‐Head Coordination During Smooth Pursuit
2.1 Summary and Comparison of Visually Triggered and Smooth Pursuit Strategies
3 Other Strategies of Eye‐Head Coordination
4 Plastic Changes in Central Organization of Eye‐Head Coordination
4.1 Centrally Generated Slow Phases
4.2 Modification of Saccades
Figure 1. Figure 1.

Comparison of eye saccades and gaze. A: eye saccade to a suddenly appearing target with head fixed. B: coordinated eye saccade (E) and head movement (H) to same target with head free. Gaze movement (G) represents sum of E and H. Note remarkable similarity of eye saccade in A and gaze trajectory in B as well as reduced saccade amplitude in B. Time calibration, 100 ms.

From Morasso, Bizzi, and Dichgans 85
Figure 2. Figure 2.

Amplitude, duration, and peak velocity of eye saccades and gaze. The abscissa represents the angular distance between starting position of eyes and target position. ▴—‐▴, Saccades during continuous immobilization of the head; ◯—‐◯, gaze movements; •—‐•, saccades during head turning. Each point represents mean of 20 measurements from 3 adult monkeys studied with standard deviations.

From Morasso, Bizzi, and Dichgans 85
Figure 3. Figure 3.

Eye‐head coordination triggered by sequential appearance of targets spaced by 20°. Note decrease in saccade amplitude versus gaze.

From Morasso, Bizzi, and Dichgans 85
Figure 4. Figure 4.

A: typical coordinated eye (e) and head (h) response to sudden appearance of a target. B: presentation of the same target is followed by application of the brake (horizontal bar). Note lack of compensatory eye movement. Dots represent onset of luminous target. Calibration: horizontal bar equals 500 ms; vertical bar, 15°.

From Bizzi et al. 17. Copyright 1971 by the American Association for the Advancement of Science
Figure 5. Figure 5.

Triggered eye‐head coordination. Electromyographic activity recorded from left lateral rectus (B) and right (D) and left (E) splenii capitis during horizontal eye‐head turning. Horizontal eye movements (A); horizontal head movements (C). Arrow represents onset of luminous target. Time calibration, 100 ms; eye calibration, 10°; head calibration, 20°.

From Bizzi et al. 122
Figure 6. Figure 6.

Characteristics of head movement during the triggered mode. A fixation target in the center is shortly followed by a peripheral one at 20°, 30°, and 40°. A: amplitude of head (H) movement versus target displacement for two monkeys. B: peak of head velocity versus amplitude of head movement for the same monkeys. In both figures circles and squares represent the average of at least 10 measurements with their standard deviation.

From Bizzi et al. 122
Figure 7. Figure 7.

Scanning movement. Upper trace, horizontal eye movements; middle trace, horizontal head movement; lower trace, head velocity. Note modulation of head velocity synchronous with saccadic eye movements. Time calibration, 500 ms.

From Bizzi et al. 122
Figure 8. Figure 8.

Visually triggered head movements in chronically vestibulectomized monkey. A: preoperative: an unloaded head movement (left) is compared with loaded head movement (right). Note the head returns to the same final position after removal of the load. EMG, electromyographic activity recorded from left and right splenii capitis. B: after cervical and thoracic dorsal root section (C1–Th2). Note slowing down of loaded head movement and cocontractions. Both unloaded and loaded movements elicited by the appearance of target, but performed in total darkness.

From Bizzi et al. 15
Figure 9. Figure 9.

Schematic, visually triggered movement.
Figure 10. Figure 10.

Pursuit with combined eye and head movement. Pursuit movements of eye and head are shown together with computed gaze and retinal error. The target, which periodically reverses direction, is superimposed on both head and gaze tracings. Head pursued target, while eyes remained relatively close to center of orbit. There is no obvious difference between the retinal error pattern recorded here and that observed in monkeys whose heads were restrained.

From Lanman, Bizzi, and Allum 70
Figure 11. Figure 11.

The brake experiment. Result of suddenly and unexpectedly stopping head movement (H) during ongoing pursuit in the normal monkey. Before application of brake, head tracks target (TARG), and eyes (E) remain fairly stationary in the orbit. When head is braked, eyes start to move so that there is no detectable change in gaze velocity or retinal error (RE).

Adapted from Lanman, Bizzi, and Allum 70
Figure 12. Figure 12.

Schematic, smooth pursuit movement.
Figure 13. Figure 13.

A: eye‐head coordination triggered by the presentation of a visual stimulus (see dot at bottom). B: predictive eye‐head coordination. Target appeared after head turning (see dot at bottom). a: Horizontal eye movement; b: horizontal head movement; c: right splenii capitis; and d: left splenii capitis. Time calibration, 200 ms. Eye calibration in A, 30°; in B, 30°. Head calibration, 40°.

From Bizzi et al. 16
Figure 14. Figure 14.

Blocking experiments. Subjects 1 (left) and 2 (right). Eye, eye position in the orbit. Head, head position in space. Gaze = eye + head, eye position in space. Left, target jumps to new position at spike. It remains illuminated for about 200 ms, then is extinguished for about 1 s. Finally, it is relighted at its new position. Right, target remains continuously illuminated after changing position. Note inversion of head‐position trace. Helmet of subject was nonpredictably immobilized at the onset of a combined eye‐head movement to a nonpredictable target jump. Note preprogramming of a compensatory slow phase of much higher velocity than any residual head motion. Amplitude of saccade is also decreased.

From Kasai and Zee 65


Figure 1.

Comparison of eye saccades and gaze. A: eye saccade to a suddenly appearing target with head fixed. B: coordinated eye saccade (E) and head movement (H) to same target with head free. Gaze movement (G) represents sum of E and H. Note remarkable similarity of eye saccade in A and gaze trajectory in B as well as reduced saccade amplitude in B. Time calibration, 100 ms.

From Morasso, Bizzi, and Dichgans 85


Figure 2.

Amplitude, duration, and peak velocity of eye saccades and gaze. The abscissa represents the angular distance between starting position of eyes and target position. ▴—‐▴, Saccades during continuous immobilization of the head; ◯—‐◯, gaze movements; •—‐•, saccades during head turning. Each point represents mean of 20 measurements from 3 adult monkeys studied with standard deviations.

From Morasso, Bizzi, and Dichgans 85


Figure 3.

Eye‐head coordination triggered by sequential appearance of targets spaced by 20°. Note decrease in saccade amplitude versus gaze.

From Morasso, Bizzi, and Dichgans 85


Figure 4.

A: typical coordinated eye (e) and head (h) response to sudden appearance of a target. B: presentation of the same target is followed by application of the brake (horizontal bar). Note lack of compensatory eye movement. Dots represent onset of luminous target. Calibration: horizontal bar equals 500 ms; vertical bar, 15°.

From Bizzi et al. 17. Copyright 1971 by the American Association for the Advancement of Science


Figure 5.

Triggered eye‐head coordination. Electromyographic activity recorded from left lateral rectus (B) and right (D) and left (E) splenii capitis during horizontal eye‐head turning. Horizontal eye movements (A); horizontal head movements (C). Arrow represents onset of luminous target. Time calibration, 100 ms; eye calibration, 10°; head calibration, 20°.

From Bizzi et al. 122


Figure 6.

Characteristics of head movement during the triggered mode. A fixation target in the center is shortly followed by a peripheral one at 20°, 30°, and 40°. A: amplitude of head (H) movement versus target displacement for two monkeys. B: peak of head velocity versus amplitude of head movement for the same monkeys. In both figures circles and squares represent the average of at least 10 measurements with their standard deviation.

From Bizzi et al. 122


Figure 7.

Scanning movement. Upper trace, horizontal eye movements; middle trace, horizontal head movement; lower trace, head velocity. Note modulation of head velocity synchronous with saccadic eye movements. Time calibration, 500 ms.

From Bizzi et al. 122


Figure 8.

Visually triggered head movements in chronically vestibulectomized monkey. A: preoperative: an unloaded head movement (left) is compared with loaded head movement (right). Note the head returns to the same final position after removal of the load. EMG, electromyographic activity recorded from left and right splenii capitis. B: after cervical and thoracic dorsal root section (C1–Th2). Note slowing down of loaded head movement and cocontractions. Both unloaded and loaded movements elicited by the appearance of target, but performed in total darkness.

From Bizzi et al. 15


Figure 9.

Schematic, visually triggered movement.



Figure 10.

Pursuit with combined eye and head movement. Pursuit movements of eye and head are shown together with computed gaze and retinal error. The target, which periodically reverses direction, is superimposed on both head and gaze tracings. Head pursued target, while eyes remained relatively close to center of orbit. There is no obvious difference between the retinal error pattern recorded here and that observed in monkeys whose heads were restrained.

From Lanman, Bizzi, and Allum 70


Figure 11.

The brake experiment. Result of suddenly and unexpectedly stopping head movement (H) during ongoing pursuit in the normal monkey. Before application of brake, head tracks target (TARG), and eyes (E) remain fairly stationary in the orbit. When head is braked, eyes start to move so that there is no detectable change in gaze velocity or retinal error (RE).

Adapted from Lanman, Bizzi, and Allum 70


Figure 12.

Schematic, smooth pursuit movement.



Figure 13.

A: eye‐head coordination triggered by the presentation of a visual stimulus (see dot at bottom). B: predictive eye‐head coordination. Target appeared after head turning (see dot at bottom). a: Horizontal eye movement; b: horizontal head movement; c: right splenii capitis; and d: left splenii capitis. Time calibration, 200 ms. Eye calibration in A, 30°; in B, 30°. Head calibration, 40°.

From Bizzi et al. 16


Figure 14.

Blocking experiments. Subjects 1 (left) and 2 (right). Eye, eye position in the orbit. Head, head position in space. Gaze = eye + head, eye position in space. Left, target jumps to new position at spike. It remains illuminated for about 200 ms, then is extinguished for about 1 s. Finally, it is relighted at its new position. Right, target remains continuously illuminated after changing position. Note inversion of head‐position trace. Helmet of subject was nonpredictably immobilized at the onset of a combined eye‐head movement to a nonpredictable target jump. Note preprogramming of a compensatory slow phase of much higher velocity than any residual head motion. Amplitude of saccade is also decreased.

From Kasai and Zee 65
References
 1. Abrahams, V. C. The physiology of neck muscles; their role in head movement and maintenance of posture. Can. J. Physiol. Pharmacol. 55: 332–338, 1977.
 2. Abrahams, V. C., and S. Falchetto. Hind leg ataxia of cervical origin and cervico‐lumbar spinal interactions with a supratentorial pathway. J. Physiol. London 203: 435–447, 1969.
 3. Abrahams, V. C., and P. K. Rose. Projections of extraocular, neck muscle, and retinal afferents to superior colliculus in the cat: their connections to cells of origin of the tectospinal tract. J. Neurophysiol. 38: 10–18, 1975.
 4. Allum, J. H. J. Responses to load disturbances in human shoulder muscles: the hypothesis that one component is a pulse test information signal. Exp. Brain Res. 22: 307–326, 1975.
 5. Altman, J., and M. B. Carpenter. Fiber projection of the superior colliculus in the cat. J. Comp. Neurol. 116: 157–177, 1961.
 6. Anderson, M. E. Segmental reflex inputs to motoneurons innervating dorsal neck musculature in the cat. Exp. Brain Res. 28: 175–187, 1977.
 7. Anderson, M. E., M. Yoshida, and V. J. Wilson. Influence of superior colliculus on cat neck motoneurons. J. Neurophysiol. 34: 898–907, 1971.
 8. Atkin, A., and M. B. Bender. Ocular stabilization during oscillatory head movements. Arch. Neurol. 19: 559–566, 1968.
 9. Baker, R. G., W. Precht, and R. Llinás. Cerebellar modulatory action on the vestibulo‐trochlear pathways in cat. Exp. Brain Res. 5: 364–385, 1972.
 10. Bárány, R. Augenbewegungen, durch Thoraxbewegungen auslöst. Zentralbl. Physiol. 20: 298–302, 1906.
 11. Barnes, G. R. Vestibulo‐ocular function during co‐ordinated head and eye movements to acquire visual targets. J. Physiol. London 287: 127–147, 1979.
 12. Barr, C. C., L. W. Schultheis, and D. A. Robinson. Voluntary, non‐visual control of the human vestibulo‐ocular reflex. Acta Otolaryngol. 81: 365–375, 1976.
 13. Bartz, A. E. Eye and head movements in peripheral vision: nature of compensatory eye movements. Science 152: 1644–1645, 1966.
 14. Bizzi, E. Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp. Brain Res. 6: 69–80, 1968.
 15. Bizzi, E., P. Dev, P. Morasso, and A. Polit. Effect of load disturbances during centrally initiated movements. J. Neurophysiol. 41: 542–556, 1978.
 16. Bizzi, E., R. E. Kalil, and P. Morasso. Two modes of active eye‐head coordination in monkeys. Brain Res. 40: 45–48, 1972.
 17. Bizzi, E., R. E. Kalil, P. Morasso, and V. Tagliasco. Central programming and peripheral feedback during eye‐head coordination in monkeys. In: Cerebral Control of Eye Movements and Motion Perception, edited by J. Dichgans and E. Bizzi. Basel: Karger, 1972, p. 220–232.
 18. Bizzi, E., R. E. Kalil, and V. Tagliasco. Eye‐head coordination in monkeys: evidence for centrally patterned organization. Science 173: 452–454, 1971.
 19. Bizzi, E., A. Polit, and P. Morasso. Mechanisms underlying achievement of final head position. J. Neurophysiol. 39: 435–444, 1976.
 20. Bizzi, E., and P. H. Schiller. Single unit activity in the frontal eye fields of unanesthetized monkeys during eye and head movements. Exp. Brain Res. 10: 151–158, 1970.
 21. Boyle, R., and O. Pompeiano. Sensitivity of interpositus neurons to neck afferent stimulation. Brain Res. 168: 180–185, 1979.
 22. Cohen, B., and V. Henn. Unit activity in the pontine reticular formation associated with eye movements. Brain Res. 46: 403–410, 1972.
 23. Cohen, L. A. Role of eye and neck proprioceptive mechanisms in body orientation and motor coordination. J. Neurophysiol. 24: 1–11, 1961.
 24. Collewijn, H. Eye‐ and head movements in freely moving rabbits. J. Physiol. London 266: 471–498, 1977.
 25. Collewijn, H., Gaze in freely moving subjects. In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, vol. 1, p. 13–22.
 26. Cooper, S., and P. M. Daniel. Muscle spindles in man; their morphology in the lumbricals and the deep muscles of the neck. Brain 86: 563–586, 1963.
 27. Cooper, S., and M. Fillenz. Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles. J. Physiol. London 127: 400–413, 1955.
 28. Coulter, J. D., R. M. Bowker, S. P. Wise, E. A. Murray, A. J. Castiglioni, and K. N. Westlund. Cortical, tectal and medullary descending pathways to the cervical spinal cord. In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 263–279.
 29. Crommelick, M., and A. Roucoux. Characteristics of cat's eye saccades in different states of alertness. Brain Res. 103: 574–578, 1976.
 30. De Kleijn, A. Action réflexes du labyrinthe et du cou sur les muscles de l'oeil. Arch. Néerl. Physiol. 2: 644–649, 1918.
 31. De Kleijn, A. Tonische Labyrinth‐und Halsreflex auf die Augen. Pfluegers Arch. 189: 82–97, 1921.
 32. De Kleijn, A. Recherches quantitatives sur les positions compensatoires de l'oeil chez le lapin. Arch. Neerl. Physiol. 7: 138–141, 1922.
 33. Dichgans, J., E. Bizzi, P. Morasso, and V. Tagliasco. Mechanisms underlying recovery of eye‐head coordination following bilateral labyrinthectomy in monkeys. Exp. Brain Res. 18: 548–562, 1973.
 34. Dichgans, J., E. Bizzi, P. Morasso, and V. Tagliasco. The role of vestibular and neck afferents during eye‐head coordination in the monkey. Brain Res. 71: 225–232, 1974.
 35. Dichgans, J., B. Manck, and E. Wolpert. The influence of attention, vigilance and stimulus area on optokinetic and vestibular nystagmus and voluntary saccades. In: Oculomotor System and Brain Functions, edited by V. Zikmund. London: Butterworths, 1973, p. 280–294.
 36. Dijkgraaf, S. Die Augenstielbewegungen der Languste (Panulirus vulgaris). Experientia 11: 329–330, 1955.
 37. Dijkgraaf, S. Über die kompensatorischen Augenstielbewegungen bei Brachyuren. Pubbl. Stn. Zool. Napoli 28: 341–358, 1956.
 38. Donaghy, M. J. The role of vestibular feedback in the control of gaze changes accomplished by co‐ordinated eye and head movements. Exp. Brain Res. 23: (Suppl.) p. 227, 1975.
 39. Easter, S. S., Jr., and P. P. Johns. Horizontal compensatory eye movements in goldfish (Carassius auratus). II. A comparison of normal and deafferented animals. J. Comp. Physiol. 92: 37–57, 1974.
 40. Easter, S. S., Jr., P. R. Johns, and D. Heckenlively. Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J. Comp. Physiol. 92: 23–35, 1974.
 41. Ezure, K., S. Sasaki, Y. Uchino, and V. J. Wilson. Frequency‐response analysis of vestibular‐induced neck reflex in a cat. II. Functional significance of cervical afferents and polysynaptic descending pathways. J. Neurophysiol. 41: 459–471, 1978.
 42. Feldman, A. G. Change of muscle length due to shift of the equilibrium point of the muscle‐load system. Biofizika 19: 534–538, 1974.
 43. Fleming, D. G., G. W. Vossius, G. Bowman, and E. L. Johnson. Adaptive properties of the eye‐tracking system as revealed by moving‐head and open‐loop studies. Ann. NY Acad. Sci. 156: 825–850, 1969.
 44. Friedrickson, J. M., D. Schwarz, and H. H. Kornhuber. Convergence and interaction of vestibular and deep somatic afferents upon neurons in the vestibular nuclei of cat. Acta Otolaryngol. 61: 168–188, 1965.
 45. Fuchs, A. F. Saccadic and smooth pursuit eye movements in the monkey. J. Physiol. London 191: 609–31, 1967.
 46. Fukushima, K., N. G. Pitts, and B. W. Peterson. Direct excitation of neck motoneurons by interstitiospinal fibers. Exp. Brain Res. 33: 565–581, 1978.
 47. Fuller, J., Eye and head movements in the bush baby (Abstract). 12: 149, 1979. (Assoc. Res. Vision Ophthalmol. Inc., Annual Spring Meeting, Sarasota, FL., April 30‐May 4, 1979.).
 48. Funk, C. J., and M. E. Anderson. Saccadic eye movements and eye‐head coordination in children. Percept. Mot. Skills 44: 599–610, 1977.
 49. Gauthier, G. M., and D. A. Robinson. Adaptation of human vestibuloocular reflex to magnifying lenses. Brain Res. 92: 331–335, 1975.
 50. Gonshor, A., and G. Melvill‐Jones. Changes of human vestibulo‐ocular response induced by vision‐reversal during head rotation (Abstract). J. Physiol. London 234: 102P–103P, 1973.
 51. Greene, T., and R. Jampel. Muscle spindles in the extraocular muscles of the macaque. J. Comp. Neurol. 126: 547–550, 1966.
 52. Gresty, M. A. Coordination of head and eye movements to fixate continuous and intermittent targets. Vision Res. 14: 395–403, 1974.
 53. Gresty, M. A. Eye, head and body movements of the guinea pig in response to optokinetic stimulation and sinusoidal oscillation in yaw. Pfluegers Arch. 353: 201–214, 1975.
 54. Gresty, M. A. A reexamination of ‘neck reflex’ eye movements in the rabbit. Acta Otolaryngol. 81: 386–394, 1976.
 55. Grillner, S. The role of muscle stiffness in meeting the changing postural and locomotor requirements for force development by the ankle extensors. Acta Physiol. Scand. 86: 92–108, 1972.
 56. Haddad, G. M., and D. A. Robinson. Cancellation of the vestibulo‐ocular reflex during active and passive head movements in the normal cat. Soc. Neurosci. Abstr. 3: 155, 1977.
 57. Harris, H. J. Eye movements of the dogfish (Squalus acanthias). J. Exp. Biol. 43: 107–130, 1965.
 58. Harris, L. R. The superior colliculus and movements of the head and eyes in cats. J. Physiol. London 300: 367–391, 1980.
 59. Hermann, H. T., and M. Constantine. Eye movements in the goldfish. Vision Res. 11: 313–333, 1971.
 60. Highstein, S. M. Synaptic linkages in the vestibulo‐ocular and cerebello‐vestibular pathways to the VIth nucleus in the rabbit. Exp. Brain Res. 17: 301–314, 1973.
 61. Hikosaka, O., and M. Maeda. Cervical effects of abducens motoneurons and their interaction with vestibulo‐ocular reflex. Exp. Brain Res. 18: 512–530, 1973.
 62. Houk, J. C. Regulation of stiffness by skeletomotor reflexes. Annu. Rev. Physiol. 41: 99–114, 1979.
 63. Illert, M., A. Lundberg, Y. Padel, and R. Tanaka. Integration in descending motor pathways controlling the forelimb in the cat. V. Properties of and monosynaptic excitatory convergence of C3–C4 propriospinal neurons. Exp. Brain Res. 33: 101–130, 1978.
 64. Ito, M., Adaptive modification of the vestibulo‐ocular reflex in rabbits affected by visual inputs and its possible neuronal mechanisms. In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 757–761.
 65. Ito, M., T. Shiida, N. Yagi, and M. Yamamoto. The cerebellar modification of rabbit's horizontal vestibulo‐ocular reflex induced by sustaining head rotation combined with visual stimulation. Proc. Jpn. Acad. 50: 85–89, 1974.
 66. Jürgens, R., W. Becker, and P. Rieger. The programming of fast eye movements during natural vestibular stimulation. Two types of interactions. IFAC Symp. Control Mech. Bio Ecosyst. 3, Leipzig, 1977, p. 120.
 67. Kasai, T., and D. S. Zee. Eye‐head coordination in labyrinthine‐defective human beings. Brain Res. 144: 123–141, 1978.
 68. Keller, E. L. Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res. 24: 459–471, 1976.
 69. Keller, E. L. Gain of the vestibulo‐ocular reflex in monkey at high rotational frequencies. Vision Res. 18: 311–315, 1978.
 70. Kenins, P., H. Kikillus, and E. D. Schomburg. Short‐ and long‐latency reflex pathways from neck afferents to hindlimb motoneurones in the cat. Brain Res. 149: 235–238, 1978.
 71. Kommerell, G., and R. Täumer. Investigations of the eye tracking system through stabilized retinal images. In: Cerebral Control of Eye Movements and Motion Perception, edited by J. Dichgans and E. Bizzi. Basel: Karger, 1972 p. 288–297.
 72. Lanman, J., E. Bizzi, and J. Allum. The coordination of eye and head movement during smooth pursuit. Brain Res. 153: 39–53, 1978.
 73. Lindsay, K. W., T. D. Roberts, and J. R. Rosenberg. Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in the decerebrate cat. J. Physiol. London 261: 583–601, 1976.
 74. Lisberger, S., and A. Fuchs. Response of flocculus Purkinje cells to adequate vestibular stimulation in the alert monkey: fixation vs. compensatory eye movements. Brain Res. 69: 347–353, 1974.
 75. Lorente de nó, R. Vestibulo‐ocular reflex. Arch. Neurol. Psychiatry 30: 245–291, 1933.
 76. Luschei, E. S., and A. F. Fuchs. Activity of brain stem neurons during eye movements of alert monkeys. J. Neurophysiol. 35: 445–461, 1972.
 77. Magnus, R. Koerperstellung. Berlin: Springer‐Verlag, 1924.
 78. Magnus, R., and A. De Kleijn. Die Abhängigkeit des Tonus der Extremitätenmuskeln von der Kopfstellung. Pfluegers Arch. 145: 455–548, 1912.
 79. Mandl, G., and D. Guitton. Saccadic and vestibular velocity commands: do they add? Soc. Neurosci. Abstr. 4: 165, 1978.
 80. Manni, E., and R. Bortolami. Peripheral and central organization of the extraocular muscle proprioception in the Ungulata. In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 291–299.
 81. Manni, E., R. Bortolami, V. E. Pettorossi, M. L. Lucchi, and E. Calegari. Afferent fibers and sensory ganglion cells within the oculomotor nerve in some mammals and man. II. Electrophysiological investigations. Arch. Ital. Biol. 116: 16–24, 1978.
 82. Manni, E., G. Palmieri, and R. Marini. Peripheral pathway of the proprioceptive afferents from the lateral rectus muscle of the eye. Exp. Neurol. 30: 46–53, 1971.
 83. McCouch, G. P., I. D. Deering, and T. H. Ling. Location of receptors for tonic neck reflexes. J. Neurophysiol. 14: 191–195, 1951.
 84. Meiry, L. J., Vestibular and propioceptive stabilization of eye movements. In: The Control of Eye Movement, edited by P. Bach‐y‐Rita, C. C. Collins, and J. E. Hyde. NY: Academic, 1971, p. 483–496.
 85. Miles, F. A., and J. H. Fuller. Visual tracking and the primate flocculus. Science 189: 1000–1002, 1975.
 86. Miles, F. A., and J. H. Fuller. Adaptive plasticity in the vestibulo‐ocular responses of the rhesus monkey. Brain Res. 80: 512–516, 1976.
 87. Morasso, P., E. Bizzi, and J. Dichgans. Adjustment of saccade characteristics during head movements. Exp. Brain Res. 16: 492–500, 1973.
 88. Morasso, P., G. Sandini, V. Tagliasco, and R. Zaccaria. Control strategies in eye‐head coordination system. IEEE Trans. Syst. Man Cybern. SMC‐7: 639–651, 1977.
 89. Nyberg‐Hansen, R. The location and termination of tectospinal fibers in the cat. Exp. Neurol. 9: 212–227, 1964.
 90. Peterson, B. W., N. G. Pitts, and K. Fukushima. Reticulospinal connections with limb and axial motoneurons. Exp. Brain Res. 36: 1–20, 1979.
 91. Pompeiano, O., and A. Brodal. Spino‐vestibular fibers in the cat. J. Comp. Neurol. 108: 353–362, 1957.
 92. Puckett, J., and R. M. Steinman. Tracking eye movements with and without saccadic correction. Vision Res. 9: 695–703, 1969.
 93. Rapoport, S. Reflex connexions of motoneurones of muscles involved in head movement in the cat. J. Physiol. London 289: 311–327, 1979.
 94. Rapoport, S., A. Susswein, Y. Uchino, and V. J. Wilson. Synaptic actions of individual vestibular neurones on cat neck motoneurones. J. Physiol. London 272: 367–382, 1977.
 95. Rashbass, C. The relationship between saccadic and smooth tracking eye movements. J. Physiol. London 159: 326–338, 1961.
 96. Richmond, F. J. R. Physiological characteristics of neck muscle receptors in the cat (Abstract). J. Physiol. London 272: 67P–68P, 1977.
 97. Richmond, F. J. R., and V. C. Abrahams. Morphology and distribution of muscle spindles in dorsal muscles of the cat neck. J. Neurophysiol. 38: 1322–1339, 1975.
 98. Richmond, F. J. R., and V. C. Abrahams. What are the proprioceptors of the neck? In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 245–254.
 99. Richmond, F. J. R., G. C. B. Anstee, E. A. Sherwin, and V. C. Abrahams. Motor and sensory fibres of neck muscle nerves in the cat. Can. J. Physiol. Pharmacol. 54: 294–304, 1976.
 100. Richmond, F. J. R., D. A. Lakanen, and V. C. Abrahams. Receptors around vertebrae in the cat neck. Soc. Neurosci. Abstr. 4: 518, 1978.
 101. Roberts, T. D. M. Neurophysiology of Postural Mechanisms (2nd ed.). London: Butterworths, 1978.
 102. Robinson, D. A. The mechanics of human saccadic eye movement. J. Physiol. London 174: 245–264, 1964.
 103. Robinson, D. A. Adaptive gain control of vestibuloocular reflex by the cerebellum. J. Neurophysiol. 39: 954–969, 1976.
 104. Robinson, D. L., and C. D. Jarvis. Superior colliculus neurons studied during head and eye movements of the behaving monkey. J. Neurophysiol. 37: 533–540, 1974.
 105. Rose, P. K., and N. Sprott. Proprioceptive and somatosensory influences on neck muscle motoneurons. In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 255–262.
 106. Roucoux, A., M. Crommelinck, and M. Meulders. Visual fixation: a collicular reflex? In: Progress in Brain Research. Reflex Control of Posture and Movement, edited by R. Granit and O. Pompeiano. Amsterdam: Elsevier, 1979, vol. 50, p. 745–753.
 107. Schaefer, K.‐P., D. L. Meyer, U. Buttner, and D. Schott. The effect of head position on oculomotor discharge patterns in rabbits. In: Basic Mechanisms of Ocular Motility and Their Clinical Implications, edited by G. Lennerstrand and P. Bachy‐Rita. New York: Pergamon, 1975, p. 457–459.
 108. Sherrington, C. S. Flexion‐reflex of the limb, crossed extension‐reflex and reflex stepping and standing. J. Physiol. London 40: 28–121, 1910.
 109. Stark, L., G. Vossius, and L. R. Young. Predictive control of eye tracking movements. IEEE Trans. Hum. Factors Electron. HFE‐3: 52–57, 1962.
 110. Stryker, M. P., and P. H. Schiller. Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp. Brain Res. 23: 103–112, 1975.
 111. Sugie, N., and G. Melvill‐Jones. A model of eye movements induced by head rotation. IEEE Trans. Syst. Man Cybern. SMC‐1: 251–260, 1971.
 112. Sugie, N., and M. Wakakuwa. Visual target tracking with active head rotation. IEEE Trans. Syst. Sci. Cybern. SSC‐6: 103–109, 1970.
 113. Szentágothai, J. The elementary vestibulo‐ocular reflex arc. J. Neurophysiol. 13: 395–407, 1950.
 114. Takemori, S., and J.‐I. Suzuki. Eye deviations from neck torsion in humans. Ann. Otol. Rhinol. Laryngol. 80: 439–444, 1971.
 115. Tozer, F. M., and C. S. Sherrington. Receptors and afferents of the third, fourth and sixth cranial nerves. Proc. R. Soc. London Ser. B 82: 450–457, 1910.
 116. Vallbo, Å. B., The significance of intramuscular receptors in load compensation during voluntary contractions in man. In: Control of Posture and Locomotion, edited by R. B. Stein, K. G. Pearson, R. S. Smith, and J. B. Redford, New York: Plenum, 1974, p. 211–226.
 117. Waespe, W., and V. Henn. Neuronal activity in the vestibular nuclei in the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res. 27: 523–538, 1977.
 118. Warabi, T. Trunk‐ocular reflex in man. Neurosci. Lett. 9: 267–270, 1978.
 119. Westheimer, G., and S. M. Blair. Oculomotor defects in cerebellectomized monkeys. Invest. Ophthalmol. 12: 618–621, 1973.
 120. Wilson, V. J., and M. Maeda. Connections between semicircular canals and neck motoneurons in the cat. J. Neurophysiol. 30: 346–357, 1974.
 121. Yasui, S., and L. Young. Perceived visual motion as effective stimulus to pursuit eye movement system. Science 190: 906–908, 1975.
 122. Young, L. R., Pursuit eye movement—what is being pursued? In: Control of Gaze by Brain Stem Neurons, edited by R. Baker and A. Berthoz. Amsterdam: Elsevier, 1977, vol. 1, p. 29–36.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Eye‐Head Coordination
 

How to Cite

Emilio Bizzi. Eye‐Head Coordination. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 1321-1336. First published in print 1981. doi: 10.1002/cphy.cp010229