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  • Review Article
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The brainstem control of saccadic eye movements

Nature Reviews Neuroscience volume 3, pages 952–964 (2002)Cite this article

Key Points

  • The oculomotor system is a useful model for the study of purposeful movements. Rotations of the eyes are produced by three pairs of extraocular muscles that are innervated by motor neurons from the III, IV and VI cranial nerve nuclei. A saccadic eye movement is produced when the appropriate motor neurons produce a burst of spikes, followed by tonic firing at the correct rate to maintain the eye's new position.

  • The commands for horizontal components of saccades originate in the pons and medulla. Omnipause neurons fire tonically during fixation, but stop firing during saccades; long-lead burst neurons and excitatory burst neurons fire before and during saccades. Excitatory burst neurons synapse onto motor neurons and drive the motor neuron pulse of activity. Neurons in the prepositus and vestibular nuclei fire tonically and drive the step of activity that maintains eye position. Microstimulation of neurons in the pontine reticular formation produces horizontal eye movements. Neurons in the rostral midbrain that have similar properties drive vertical eye movements. The duration and velocity of saccades are determined by the duration and maximal firing rate of the bursts of activity produced by these neurons.

  • The horizontal and vertical components of oblique saccades are coordinated. The shorter of the two components proceeds at a lower velocity than normal so that the two will have the same duration and the movement will not be curved. The onsets of the two components are coordinated by omnipause neurons in the pons.

  • The torsional component of saccadic eye movements is stereotyped and obeys Donders' law: for any direction of the line of sight, if the head is upright and stationary, the eye will assume a given degree of torsion, regardless of the route taken by the eye to reach its position. Saccades also obey Listing's law, which specifies the orientation of the globe for each gaze position. It is unclear how these laws are implemented, but identifying the mechanisms is an important part of understanding the generation of saccades.

  • Neurons in the superior colliculus (SC) provide the main input to the pontine and midbrain pulse–step generators. Microstimulation of these neurons produces saccades in head-restrained animals, and coordinated head and eye movements in head-unrestrained animals. The size and direction of the movements produced are primarily determined by the position of the stimulation in the SC.

  • Models of saccade generation assume that saccades are under feedback control and that the feedback comes from corollary discharge. Models differ in the implementation of this feedback, but it has not been possible to determine the type of feedback signal used or the site of the comparator. Reasons for this include the fact that signals that are separate in models might be intermingled in the brain, preventing selective lesioning of these signals, and that different models produce similar signals. Models also tend to use population signals, but in terms of electrophysiology, it is hard to know what the population signal is at any given time. The problems faced by oculomotor researchers are mirrored in other areas of systems neuroscience.

Abstract

The modern era of oculomotor research began with the advent of the chronic single-unit recording method in the late 1960s. Research carried out in the intervening years has made it possible to provide a detailed description of the saccadic command signals that are generated by motor neurons and the formation of these signals in premotor brainstem regions. These findings have been assimilated in control-systems models that simulate important behavioural features of saccades. Despite these great advances, key issues, such as the nature of the feedback signal and the location of the comparator, are unresolved and some of the factors that have impeded progress can be identified.

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Figure 1: Extraocular muscles and typical activity of motor neurons.
Figure 2: Location and connections of brainstem saccade-related neurons.
Figure 3: The PPRF controls the horizontal component of saccades.
Figure 4: Control of torsional rotations.
Figure 5: Comparison of PPRF and collicular control of saccades.
Figure 6: Position and displacement models of saccade generation.
Figure 7: Saccade-related hyperpolarization in OPNs.
Figure 8: Activity of motor neurons innervating agonist and antagonist muscles before and during a saccade.

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Acknowledgements

This work was supported by grants from the National Institutes of Health.

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  1. Division of Neuroscience, Baylor College of Medicine, Houston, 77030, Texas, USA

    David L. Sparks

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FURTHER INFORMATION

Encyclopedia of Life Sciences

oculomotor system

MIT Encyclopedia of Cognitive Sciences

eye movements and visual attention

oculomotor control

Glossary

PLANT

A term used in control theory to refer to that which is controlled. In the case of eye movements, the oculomotor plant refers to the globe, extraocular muscles, orbital suspensory tissues and any other passive orbital tissues that influence rotation of the eye.

CYCLOROTATION

Rotations around the anteroposterior axis of the globe are known as cycloductions or cyclorotations.

ON-DIRECTION

The direction of movement associated with the maximal discharge of a neuron.

NON-COMMUTATIVITY

Having the property that the results of a mathematical operation on elements might produce different results depending on the order in which the elements are used.

LISTING'S LAW OPERATOR

A hypothetical neural circuit that performs the computations required to implement Listing's law.

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Sparks, D. The brainstem control of saccadic eye movements. Nat Rev Neurosci 3, 952–964 (2002). https://doi.org/10.1038/nrn986

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