The characteristics and neuronal substrate of saccadic eye movement plasticity
Introduction
In this review, we consider the characteristics and neuronal substrate of an example of motor learning in a voluntary behavior, the saccadic eye movement, which redirects gaze rapidly from one location to another. The saccade is an excellent movement by which to study motor adaptation because it can be manipulated behaviorally, its characteristics have been documented extensively, and its neuronal substrate may be better known than that of any other motor response. Because the saccade remains accurate despite the pressures of growth, injury and aging, the central nervous system must have a mechanism to adjust and maintain the amplitude and/or direction of saccades under changing behavioral conditions. This motor learning is called saccadic adaptation.
We divide our consideration of saccadic adaptation into three parts. First, we describe some of the different types of saccade and their possible neuronal substrates. This background information identifies the neuronal circuitry believed to subserve the various types of saccade and thus constrains the possible loci of adaptation. Second, we consider the characteristics of both natural and behavioral saccadic adaptation. Third, we discuss the behavioral and neurophysiological experiments that attempt to localize the site(s) of adaptation within the saccadic control system. Because the accuracy of saccades is most important in foveate animals and the behavioral manipulations that elicit saccades require diligent cooperation on the part of the subject, all of our knowledge to date has come from studies on primates, both humans and monkeys. Where experiments on the two primate species address similar topics, we will discuss them together.
Section snippets
Types of saccade
Primates use the fast, accurate saccade to look at objects of interest (targets) in their visual environment. Under natural conditions, most targets are stationary and we make a series of scanning saccades in rapid succession to peruse them. If a target suddenly appears in the visual field, a targeting saccade is made reactively towards it. If a target suddenly begins to move slowly, a catch-up saccade brings the target onto the fovea whereupon smooth-pursuit eye movements keep it there.
Saccadic circuitry
Several neural structures and pathways have been implicated in the generation of saccades (Fig. 2; for comprehensive reviews, see Moschovakis et al., 1996, Scudder et al., 2002). The six extraocular muscles of each eye are innervated by motoneurons located in the III, IV, and VI cranial nuclei. To generate a horizontal saccade directed laterally, for example, motoneurons in the VI nucleus discharge a burst of spikes that begins a few milliseconds before the saccade starts and ends a few
Saccadic adaptation
The majority of saccadic eye movements are quite accurate to targets that appear within about ±15° of straight-ahead, and their metrics, i.e., amplitude, duration and peak velocity, are stereotyped (Becker, 1989). In the somatomotor system, movements are slow enough that visual feedback can help guide them if the movement becomes inaccurate. Saccades, however, are extremely brief (in humans a 10° saccade lasts only about 40 ms; Becker, 1989), so visual feedback cannot be used to guide the
Motor versus sensory
Adaptation of either the amplitude or direction of saccades could be largely a motor event that occurs after sensory signals about target location have been converted into a motor command. Alternatively, adaptation could affect the neuronal representation of the visual field. For example, a 10° target step in a 20% amplitude-reduction experiment would appear to be located at an 8° eccentricity. In this scenario, an 8° saccade accurately reflects the remapped visual world caused by a sensory
Conclusion
Most of our understanding about the neuronal mechanisms underlying motor learning is the result of experiments on motor reflexes such as the blink reflex and the vestibulo-ocular reflex. This review demonstrates that the saccadic system provides a unique opportunity to study motor learning of a voluntary, precise movement. Saccadic adaptation, at least the rapid component, occurs over a short period of time so that single units may be recorded while the adaptation actually is occurring. Because
Acknowledgements
This review was supported by a predoctoral training grant (T32 EY07031-26) to JJH and NIH grants EY00745-32 and RR00166. We appreciate the incisive comments of S. Brettler, Y. Iwamoto, C. Kaneko, T. Knight, L. Ling, J. Phillips, F. Robinson, R. Soetedjo and N. Takeichi on an earlier version of this manuscript. Finally, we gratefully acknowledge the deft editorial assistance of K. Elias.
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