Dynamic overshoot in saccadic eye movements is caused by neurological control signal reversals

doi:10.1016/0014-4886(75)90226-5

Experimental Neurology

Volume 48, Issue 1, July 1975, Pages 107-122

https://doi.org/10.1016/0014-4886(75)90226-5 Get rights and content

Abstract

Three quite different types of overshoot occur in saccadic eye movements; each has unique characteristics determined by distinct neuronal control patterns. Most saccades have dynamic overshoot; it is more prevalent among, and more prominent in, small saccades. Dynamic overshoot is caused by nonrandom reversals of the neuronal control signals. It is a monocular phenomenon. The return velocities for dynamic overshoot are equal to saccadic velocities and are much larger than vergence velocities.

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While not incorporated in the models of Figs. 2 and 4, Stark, Bahill and colleagues have pointed out that in a predominately second-order system, active braking (a small reversed pulse just at the end of the saccade) can bring the eye quickly to rest and act as a so-called time-optimal input signal. This idea is correct on theoretical grounds (e.g., Clark and Stark, 1975), and, evidently, on experimental grounds as well (Bahill et al., 1975), although the pulse actually seen is tiny compared to what these authors anticipated. Here again, the models (Figs. 2 and 4) produced correct saccades in the absence of a component of the input signal subsequently declared by their authors to be important.
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This chapter discusses the premotor neural mechanisms that control horizontal saccadic eye movements. Oculomotoneurons carry a pulse-step signal that underlies the pulse-step force driving the overdamped plant. The pulse and step are both generated by a common signal, arising from medium-lead burst neurons in the pons. Their burst signal encodes saccadic eye velocity, while the number of spikes in the burst relates to the saccade amplitude. The step component, which encodes the eye position, is obtained by neural integration of the burst. Several oculomotor neural disorders can be explained by impairments in the binocular push-pull organization of this pulse-step mechanism. Plasticity of the pulse-step control, e.g., in response to muscle weakening, is mediated by cerebellar vermis and flocculus. Saccadic offset may be controlled, either by active braking, or by an exponential slide signal. The neurophysiology is summarized by a quantitative model, in which the firing rate of burst neurons is controlled by a dynamic negative feedback loop that carries the instantaneous eye position signal from the neural integrator. This signal is compared with a desired eye-position command in the head from higher centers, and the resulting dynamic motor error drives the high-gain burst cells. Instability of the system is prevented by the mutual inhibitory interaction between burst cells and omnipause neurons. The model explains many features of normal saccades, but also accounts for pathologies and abnormalities like dynamic overshoots and saccade oscillations.
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Previous research has demonstrated that the distraction caused by holding a mobile telephone conversation is not limited to the period of the actual conversation (Haigney, 1995; Redelmeier & Tibshirani, 1997; Savage et al., 2013). In a prior study we identified potential eye movement and EEG markers of cognitive distraction during driving hazard perception. However the extent to which these markers are affected by the demands of the hazard perception task are unclear. Therefore in the current study we assessed the effects of secondary cognitive task demand on eye movement and EEG metrics separately for periods prior to, during and after the hazard was visible. We found that when no hazard was present (prior and post hazard windows), distraction resulted in changes to various elements of saccadic eye movements. However, when the target was present, distraction did not affect eye movements.
We have previously found evidence that distraction resulted in an overall decrease in theta band output at occipital sites of the brain. This was interpreted as evidence that distraction results in a reduction in visual processing. The current study confirmed this by examining the effects of distraction on the lambda response component of subjects eye fixation related potentials (EFRPs). Furthermore, we demonstrated that although detections of hazards were not affected by distraction, both eye movement and EEG metrics prior to the onset of the hazard were sensitive to changes in cognitive workload. This suggests that changes to specific aspects of the saccadic eye movement system could act as unobtrusive markers of distraction even prior to a breakdown in driving performance.
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Recent research have shown that the eye movement data measured by an eye tracker does not necessarily reflect the exact rotations of the eyeball. For example, post-saccadic eye movements may be more reflecting the relative movements between the pupil and the iris rather than the eyeball oscillations. Since, accurate measurement of eye movements is important in many studies, it is crucial to identify different factors that influence the dynamics of the eye movements measured by an eye tracker. Previous studies have shown that deformation of the internal structure of the iris and size of the pupil directly affect the amplitude of the post-saccadic oscillations that are measured by video-based eye trackers that are pupil-based. In this paper, we look at the effect of aging on post-saccadic oscillations. We recorded eye movements from a group of 43 young and 22 older participants during an abstract and a more natural viewing task. The recording was conducted with a video-based eye tracker using the pupil center and corneal reflection. We anticipated that changes in the muscle strength as an effect of aging might affect, directly or indirectly, the post-saccadic oscillations. Results showed that the size of the post-saccadic oscillations were significantly larger for our older group. The results suggests that aging has to be considered as an important factor when studying the post-saccadic eye movements.
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Gain (ratio of initial saccade amplitude to final eye position on target) was computed for each centrifugal and centripetal saccade, and the gain SD (gain variation) was computed in each subject for both centrifugal and centripetal saccades. As ULD saccade gains differed from those in the HV and because the VPeak depends on saccade amplitude [28], the VPeak of six amplitudes (9°–14°) were collected. The quality of fixation was also analyzed with the square-wave jerk (horizontal saccadic intrusions) frequency (SWJF) counted during central fixation.
Unverricht–Lundborg disease (ULD) is the most common form of progressive myoclonus epilepsy. Cerebellar dysfunction may appear over time, contributing along with myoclonus to motor disability. The purpose of the present work was to clarify the motor and neurophysiological characteristics of ULD patients.
Nine patients with genetically proven ULD were evaluated clinically (medical history collected from patient charts, the Scale for the Assessment and Rating of Ataxia and Unified Myoclonus Rating Scale). Neurophysiological investigations included EEG, surface polymyography, long-loop C-reflexes, somatosensory evoked potentials, EEG jerk-locked back-averaging (JLBA) and oculomotor recordings. All patients underwent brain MRI. Non-parametric Mann-Whitney tests were used to compare ULD patients’ oculomotor parameters with those of a matched group of healthy volunteers (HV).
Myoclonus was activated by action but was virtually absent at rest and poorly induced by stimuli. Positive myoclonus was multifocal, often rhythmic and of brief duration, with top-down pyramidal temporospatial propagation. Cortical neurophysiology revealed a transient wave preceding myoclonus on EEG JLBA (n = 8), enlarged somatosensory evoked potentials (n = 7) and positive long-loop C-reflexes at rest (n = 5). Compared with HV, ULD patients demonstrated decreased saccadic gain, increased gain dispersion and a higher frequency of hypermetric saccades associated with decreased peak velocity.
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Are high lags of accommodation in myopic children due to motor deficits?
2017, Vision Research
Citation Excerpt :
Studies on adults showed atypical patterns such as the dynamic overshoots and oscillations in saccades (Bahill, Clark, & Stark, 1975; Bahill, Hsu, & Stark, 1978; Doslak, Dell’osso, & Daroff, 1983; Zee, Robinson, & Eng, 1979). These atypical patterns were predicted to be due to either an unstable (Zee et al., 1979) or an inaccurate pulse generator (Bahill et al., 1975). Also, atypical patterns like the double step responses found here were shown to exist with the vergence system (Alvarez, Semmlow, Yuan, & Munoz, 2000; Semmlow, Hung, Horng, & Ciuffreda, 1994).
Children with a progressing myopia exhibit an abnormal pattern of high accommodative lags coupled with high accommodative convergence (AC/A) and high accommodative adaptation. This is not predicted by the current models of accommodation and vergence. Reduced accommodative plant gain and reduced sensitivity to blur have been suggested as potential causes for this abnormal behavior. These etiologies were tested by altering parameters (sensory, controller and plant gains) in the Simulink model of accommodation. Predictions were then compared to the static and dynamic blur accommodation (BA) measures taken using a Badal optical system on 12 children (6 emmetropes and 6 myopes, 8–13 years) and 6 adults (20–35 years). Other critical parameters such as CA/C, AC/A, and accommodative adaptation were also measured. Usable BA responses were classified as either typical or atypical. Typical accommodation data confirmed the abnormal pattern of myopia along with an unchanged CA/C. Main sequence relationship remained invariant between myopic and nonmyopic children. An overall reduction was noted in the response dynamics such as peak velocity and acceleration with age. Neither a reduced plant gain nor reduced blur sensitivity could predict the abnormal accommodative behavior. A model adjustment reflecting a reduced accommodative sensory gain (ASG) coupled with an increased AC cross-link gain and reduced vergence adaptive gain does predict the empirical findings. Empirical measures also showed a greater frequency of errors in accommodative response generation (atypical responses) in both myopic and control children compared to adults.

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¹: Dr. Clark's present address is Stanford Research Institute, Menlo Park, California 94025. We thank Dr. Robert Mandell for the soft contact lenses, and Robert Kenyon, Karen Bahill, and Cynthia Cowee for their assistance. We acknowledge partial support from NIH-GM 1418.

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Dynamic overshoot in saccadic eye movements is caused by neurological control signal reversals

Abstract

Exp. Neurol.

Brain Res.

Vision Res.

Brain Res.

Exp. Neurol.

Biophys. J.

The main sequence, a tool for studying eye movements

Math. Biosci.

Organization of vestibular nystagmus in oblique oculomotor system

J. Neurophysiol.

The control of eye movements in the saccadic system

Bibl. Ophthal.

Steps in production of motoneuron spikes during rhythmic firing

J. Neurophysiol.

Control of human eye movements

Math. Biosci.

Time optimal behavior of human saccadic eye movements

IEEE Trans. Auto. Control

The human oculomotor control system

The eye movement control signal

Dynamic behavior of human eye-positioning mechanism

Commun. Behav. Biol.

An experimental study of visual fixation

Psy Rev.

Precentral and postcentral cortical activity in association with visual triggered movement

J. Neurophysiol.

Saccadic and smooth pursuit movements in the monkey

J. Physiol.

Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement

J. Neurophysiol.

Development of isometric tension in simian extraocular muscle

J. Physiol.

Interactions between voluntary and postural mechanisms of the human motor system

J. Neurophysiol.

Feeding in Helisoma trivolvis: The morphological and physiological bases of a fixed action pattern

Amer. Zool.