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The Saccadic System

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The Saccadic System Chapter 3 The Saccadic System THE PURPOSE OF SACCADES The Role of the Basal Ganglia BEHAVIOR OF THE SACCADIC SYSTEM The Cerebellar Contribution to Saccades Saccadic Velocity and Duration MODELS FOR SACCADE GENERATION Saccadic Waveform ADAPTIVE CONTROL OF SACCADIC Saccadic Trajectory ACCURACY Saccadic Reaction Time (Latency) SACCADES AND MOVEMENTS OF THE Saccadic Accuracy EYELIDS Quantitative Aspects of Quick Phases of EXAMINATION OF SACCADES Nystagmus Clinical Examination of Saccades Ballistic Nature of Saccadic Movements Measurement of Saccadic Eye Saccades during Visual Search and Reading Movements Visual Consequences of Saccades PATHOPHYSIOLOGY OF SACCADIC NEUROPHYSIOLOGY OF SACCADIC EYE ABNORMALITIES MOVEMENTS Disorders of Saccadic Velocity Brainstem Pathways for Saccades Disorders of Saccadic Accuracy Higher-Level Control of the Saccadic Pulse Prematurely Terminated Saccades Generator Disorders of Saccadic Initiation Superior Colliculus Inappropriate Saccades: Saccadic The Role of the Frontal Lobe Intrusions and Oscillations The Role of the Parietal Lobe SUMMARY The Role of the Thalamus THE PURPOSE OF SACCADES REM sleep.782 Abnormalities of saccades are often distinctive and point to disorders of spe- Saccades are rapid eye movements that shift cific mechanisms. Thus, saccades have become the line of sight between successive points of an important research tool to study a wide fixation (Fig. 3–1). The term saccade is French range of issues in the neurosciences.392 in origin, referring to the jerking of a horse’s Dodge,157 working with J.J. Cogan, the head by a tug on the reins or to the flicking of father of David G. Cogan, in the early 20th a sail in a gust of wind. Javal334 and Landolt378 century, was the first to distinguish saccades first used the word saccade to describe the clearly from other types of eye movements. He rapid eye movements associated with reading explicitly stated their function: “to move the or voluntary changes of gaze. Saccades include eyes so that the point of interest will be seen a range of behaviors that encompass voluntary with the visual center of the retina”. Yarbus769 and involuntary shifts of fixation, quick phases emphasized the importance of saccades in of vestibular and optokinetic nystagmus, and visual search. The function of voluntary sac- the rapid eye movements that occur during cades in primates is directly linked to the pres- 108 The Saccadic System 109 ence of a fovea, because images are best seen if located there. Animals without a fovea, such as the rabbit, only make voluntary saccades in association with head movements.121,122 Afoveate animals also produce quick phases of nystagmus during passive head movements so that the slow phases of vestibular and optoki- netic nystagmus do not drive the eyes into an extreme orbital position and the oncoming visual scene can be perused. Saccadic eye movements consist of a hierar- chy of behavior, from the most rudimentary of all saccades—quick phases of vestibular nystagmus during passive rotation in darkness—through reflexive saccades made in response to the sud- den appearance of a novel visual stimulus, to higher-level volitional behavior such as saccades directed toward the remembered location of a visual target (Table 3–1). This organization can be applied in the clinical neuro-ophthalmologic examination. For example, if voluntary saccades cannot be generated, then it is useful to test pro- gressively more reflexive types of saccades down to the quick phases of nystagmus. A comparable approach is used in the neurologic localization of motor disorders of all types. BEHAVIOR OF THE SACCADIC SYSTEM Figure 3–1. Representative record of a 36-degree hori- zontal saccade made by a normal subject in response to a 40-degree target jump (dotted lines in top panel). We will discuss in turn the main characteristics Corresponding position, velocity, and acceleration records of saccades: velocity and duration, waveform for this saccade are shown. In the middle panel, compo- and trajectory, reaction time or latency, and nents of the velocity waveform are shown, including the acceleration period and total duration, the ratio of which accuracy. A number of ingenious paradigms gives a measure of the skewing of the velocity waveform. have been developed to test aspects of saccadic Positive values correspond to rightward movements. responses to visual stimuli (Fig. 3–2). Table 3–1. Classification of Saccades Classification Definition VOLITIONAL SACCADES Elective saccades made as part of purposeful behavior PREDICTIVE, ANTICIPATORY Saccades generated in anticipation of or in search of the appearance of a target at a particular location. MEMORY-GUIDED Saccades generated to a location in which a target has been previously present (Fig. 3–2C). ANTISACCADES Saccades generated in the opposite direction to the sudden appearance of a target (after being instructed to do so; Fig. 3–2D). TO COMMAND Saccades generated on cue. (Continued on following page) Table 3–1. (continued) Classification Definition REFLEXIVE SACCADES Saccades generated to novel stimuli (visual, auditory or tactile) that unexpec- edly occur within the environment. EXPRESS SACCADES Very short latency saccades that can be elicited when the novel stimulus is presented after the fixation stimulus has disappeared (gap stimulus; Fig. 3–2B) SPONTANEOUS Seemingly random saccades that occur when the subject is not required to SACCADES perform any particular behavioral task. QUICK PHASES Quick phases of nystagmus generated during vestibular or optokinetic stimula- tion or as automatic resetting movements in the presence of spontaneous drift of the eyes. Figure 3–2. Schematic of laboratory stimu- lus paradigms commonly used to test sac- cades. In each case “go” indicates the signal for the subject to look toward the “saccadic target.” (A) Overlap paradigm, in which the central fixation target stays on throughout. (B) Gap paradigm, in which fixation target is switched off before visual target is switched on. (C) Memory target task. The subject views the fixation target during the time that the visual target is flashed and after several seconds (the memory period), the fixation light is switched off and the subject looks towards the remembered location of the tar- get. (D) The antisaccade task. The subject is required to look in the opposite direction when the visual stimulus is presented. (E) Sequence of saccades task. A series of targets at several locations are turned on in turn. After a memory period, the fixation light goes out as a signal for the subject to make a series of saccades towards the remembered series of target locations. 110 The Saccadic System 111 Saccadic Velocity and Duration commonly used equation to describe the main sequence relationship is: Saccades show consistent relationships among their size, speed, and duration. Thus, the Peak velocity ϭ Vmax ϫ (1 - e-Amplitude/C) larger the saccade, the greater its top speed and the longer its duration. However, even where Vmax is the asymptotic peak velocity large saccades (Fig. 3–1) do not last much and C is a constant. Other equations, such as longer than 100 ms, which is the response time power functions, have been used to describe of the visual system. This means that visual the relationship between amplitude and peak feedback cannot be used to change the size of velocity for smaller saccades.225,385 The appli- a saccade once started. Rather, the brain must cation of this and other equations describing monitor accuracy at the end of each saccade the main sequence relationships during the and make an appropriate adjustment to ensure laboratory evaluation of saccades is discussed long-term accuracy. Representative plots of below (Measurement of Saccadic Eye Move- peak velocity or duration as a function of ments). amplitude are shown in Figure 3–3, and are The duration of saccades are approximately often referred to as main sequence relation- linearly related to their amplitudes for move- ships,38,80 a term borrowed from the classifica- ments from 1 to 50 degrees. Power functions tion of stars by astronomers. These can be used to describe the relationship relationships are consistent enough that they between amplitude and duration for saccades can be used to define ranges for normal sac- of all sizes (Fig. 3–3B).223,225,385,769 Acceleration cades; deviations of measured eye movements and its derivative, jerk, are greater than for from these intervals indicate either abnormal other types of eye movement and can be used saccades or non-saccadic eye movements. For to identify saccades.764 Saccadic speed and saccades that are smaller than about 20 duration cannot be voluntarily controlled. degrees, there is a linear relationship between However, a number of factors may cause vari- amplitude and peak velocity; above 20 degrees, ability in the peak velocity and duration of sac- peak velocity shows a progressive “soft” satura- cades of similar size, even for the same tion with asymptotic values of about 500 individual, from day to day.81 For example, sac- degrees per second. Main-sequence relation- cades are slower when made in darkness, to ships also apply to the smallest saccades the remembered locations of visual stimuli, in (microsaccades);417 these relationships are dis- anticipation of target jumps,724 and when made cussed under Visual Fixation in Chapter 4. A in the opposite direction to a visual stimulus Figure 3–3. Dynamic properties of saccades. (A) Plot of peak velocity versus amplitude of vertical saccades. Data points (dots) are saccades from 10 normal subjects. These normal data are fit with an exponential equation of the form Peak Velocity ϭ Vmax ϫ (1 - e-Amplitude/C), where Vmax is the asymptotic peak velocity, and C is a constant defining the expo- nential rise is shown. Also plotted are the 5% and 95% prediction intervals. The crossed points indicate vertical saccades from a patient with Niemann-Pick type C disease (see Fig. 5B), which lie outside the prediction intervals for normals.
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