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• W3174152900 abstract "•We classify two types of saccadic dynamic overshoot (SDO): SDOsimple and SDOcomplex•Saccades with SDO have higher peak velocity and deceleration than saccades without SDO•Elderly subjects show a higher frequency and amplitude of SDO than young subjects•Saccades with SDOcomplex occur more frequently in reflexive than voluntary saccades Saccadic eye movements may not stop steadily but fluctuate briefly, known as saccadic dynamic overshoot (SDO). The reported relationships between SDO and saccadic parameters of main saccade and the effect of aging on SDO are controversial. In addition, it is not clear whether aging-related disease, such as mild cognitive impairment (MCI) and Parkinson disease (PD), causes the specific change of SDO. To address these questions, we analyzed the spatiotemporal features of SDO in young healthy subjects, elderly healthy subjects, and subjects with PD and MCI in three oculomotor tasks. We found two types of SDOs—simple and complex SDO. We confirmed that the frequency and amplitude of SDO were positively correlated with the peak velocity and deceleration of main saccades and increased in elderly subjects; however, they were not significantly different among the three elderly groups. Our results support the previous argument that the oculomotor structure in brainstem and cerebellum directly develop SDO. Saccadic eye movements may not stop steadily but fluctuate briefly, known as saccadic dynamic overshoot (SDO). The reported relationships between SDO and saccadic parameters of main saccade and the effect of aging on SDO are controversial. In addition, it is not clear whether aging-related disease, such as mild cognitive impairment (MCI) and Parkinson disease (PD), causes the specific change of SDO. To address these questions, we analyzed the spatiotemporal features of SDO in young healthy subjects, elderly healthy subjects, and subjects with PD and MCI in three oculomotor tasks. We found two types of SDOs—simple and complex SDO. We confirmed that the frequency and amplitude of SDO were positively correlated with the peak velocity and deceleration of main saccades and increased in elderly subjects; however, they were not significantly different among the three elderly groups. Our results support the previous argument that the oculomotor structure in brainstem and cerebellum directly develop SDO. Saccades are ballistic eye movements that quickly rotate the eyes to direct the center of the retina, i.e., the fovea, to attractive objects in the visual field. Primates perform two to three saccades per second on average to help the visual system collecting high-acuity visual information (Robinson, 1964Robinson D.A. The mechanics of human saccadic eye movement.J. Physiol. 1964; 174: 245-264Crossref PubMed Scopus (563) Google Scholar). Despite the high demand of the visual system for saccades to be highly accurate, saccades do not always end precisely, e.g., saccades may not stop fully at the desired fixation point but continue to fluctuate after the main saccades. Post-saccadic instability exhibits a number of spatiotemporal profiles in both eye position and saccadic velocity, which has been referred to as saccadic dynamic overshoot (SDO), saccadic dynamic undershoot, and saccadic glissades (Enderle, 2002Enderle J.D. Neural control of saccades.Prog. Brain Res. 2002; 140: 21-49Crossref PubMed Scopus (37) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar; Nystrom et al., 2013Nystrom M. Hooge I. Holmqvist K. Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris.Vis. Res. 2013; 92: 59-66Crossref PubMed Scopus (48) Google Scholar; Van Gisbergen et al., 1981Van Gisbergen J.A. Robinson D.A. Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons.J. Neurophysiol. 1981; 45: 417-442Crossref PubMed Scopus (455) Google Scholar). Among them, SDO is the most common type (Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar) and represents the subject of the present study. SDO has been identified in humans (Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar; Cogan, 1954Cogan D.G. Ocular dysmetria - flutter-like oscillations of the eyes, and opsoclonus.Ama Arch. Ophthalmol. 1954; 51: 318-335Crossref PubMed Scopus (115) Google Scholar; Kapoula et al., 1986Kapoula Z.A. Robinson D.A. Hain T.C. Motion of the eye immediately after a saccade.Exp. Brain Res. 1986; 61: 386-394Crossref PubMed Scopus (78) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar) and nonhuman primates (Fuchs, 1967Fuchs A.F. Saccadic and smooth pursuit eye movements in the monkey.J. Physiol. 1967; 191: 609-631Crossref PubMed Scopus (237) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Van Gisbergen et al., 1981Van Gisbergen J.A. Robinson D.A. Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons.J. Neurophysiol. 1981; 45: 417-442Crossref PubMed Scopus (455) Google Scholar) by various eye-tracking techniques, including magnetic scleral search coils (Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar; Fuchs, 1967Fuchs A.F. Saccadic and smooth pursuit eye movements in the monkey.J. Physiol. 1967; 191: 609-631Crossref PubMed Scopus (237) Google Scholar; Kapoula et al., 1986Kapoula Z.A. Robinson D.A. Hain T.C. Motion of the eye immediately after a saccade.Exp. Brain Res. 1986; 61: 386-394Crossref PubMed Scopus (78) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Van Gisbergen et al., 1981Van Gisbergen J.A. Robinson D.A. Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons.J. Neurophysiol. 1981; 45: 417-442Crossref PubMed Scopus (455) Google Scholar), electrooculography (Schiller, 1970Schiller P.H. The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey.Exp. Brain Res. 1970; 10: 347-362Crossref PubMed Scopus (142) Google Scholar), video-based limbus tracking systems (Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar; Zuber et al., 1965Zuber B.L. Stark L. Cook G. Microsaccades and the velocity-amplitude relationship for saccadic eye movements.Science. 1965; 150: 1459-1460Crossref PubMed Scopus (234) Google Scholar), video-based pupil tracking systems (Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar; Nystrom et al., 2013Nystrom M. Hooge I. Holmqvist K. Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris.Vis. Res. 2013; 92: 59-66Crossref PubMed Scopus (48) Google Scholar), and video-based Purkinje image (reflexes) systems (Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar; Nystrom et al., 2013Nystrom M. Hooge I. Holmqvist K. Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris.Vis. Res. 2013; 92: 59-66Crossref PubMed Scopus (48) Google Scholar). However, the video-based eye tracking systems detect the most vigorous SDO signal compared with the other systems (Choe et al., 2016Choe K.W. Blake R. Lee S.H. Pupil size dynamics during fixation impact the accuracy and precision of video-based gaze estimation.Vis. Res. 2016; 118: 48-59Crossref PubMed Scopus (62) Google Scholar; Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar, Deubel and Bridgeman, 1995bDeubel H. Bridgeman B. Perceptual consequences of ocular lens overshoot during saccadic eye movements.Vis. Res. 1995; 35: 2897-2902Crossref PubMed Scopus (31) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar; McCamy et al., 2015McCamy M.B. Otero-Millan J. Leigh R.J. King S.A. Schneider R.M. Macknik S.L. Martinez-Conde S. Simultaneous recordings of human microsaccades and drifts with a contemporary video eye tracker and the search coil technique.PLoS One. 2015; 10: e0128428Crossref PubMed Scopus (35) Google Scholar; Nystrom et al., 2016Nystrom M. Hooge I. Andersson R. Pupil size influences the eye-tracker signal during saccades.Vis. Res. 2016; 121: 95-103Crossref PubMed Scopus (35) Google Scholar; Nystrom et al., 2013Nystrom M. Hooge I. Holmqvist K. Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris.Vis. Res. 2013; 92: 59-66Crossref PubMed Scopus (48) Google Scholar; Schmitt et al., 2007Schmitt K.U. Muser M.H. Lanz C. Walz F. Schwarz U. Comparing eye movements recorded by search coil and infrared eye tracking.J. Clin. Monit. Comput. 2007; 21: 49-53Crossref PubMed Scopus (25) Google Scholar; Traisk et al., 2005Traisk F. Bolzani R. Ygge J. A comparison between the magnetic scleral search coil and infrared reflection methods for saccadic eye movement analysis.Graefes Arch. Clin. Exp. Ophthalmol. 2005; 243: 791-797Crossref PubMed Scopus (26) Google Scholar). One reason is that, for the video-based limbus tracking and pupil tracking systems, the acceleration and deceleration of saccades are very quick, which can reach over 20,000°/s2 for a 10° saccade (Bahill et al., 1981Bahill A.T. Brockenbrough A. Troost B.T. Variability and development of a normative data base for saccadic eye movements.Invest Ophthalmol. Vis. Sci. 1981; 21: 116-125PubMed Google Scholar). During the acceleration phase of saccade, the lens lags behind the rest of the eyeball. Then during the deceleration phase, the lens movement is slowed by the elastic zonules. Therefore, after the eyeball stops rotation during a saccade, the lens still moves along the direction of saccade and overshoots the final position of eyeball and is pulled back by passive elastic forces of the zonules (Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar, Deubel and Bridgeman, 1995bDeubel H. Bridgeman B. Perceptual consequences of ocular lens overshoot during saccadic eye movements.Vis. Res. 1995; 35: 2897-2902Crossref PubMed Scopus (31) Google Scholar). Another reason is that, for the video-based Purkinje image systems, the relative movement of the iris related to the center of pupil at the end of saccade causes the post-saccadic instability (Nystrom et al., 2013Nystrom M. Hooge I. Holmqvist K. Post-saccadic oscillations in eye movement data recorded with pupil-based eye trackers reflect motion of the pupil inside the iris.Vis. Res. 2013; 92: 59-66Crossref PubMed Scopus (48) Google Scholar). Therefore, these studies argued that the SDO reflected the local motion of the lens and iris in relation to the rest of the eyeball. However, the discovery of SDO by utilizing various eye-tracking techniques reveals that, in addition to the local motion of the lens and iris, SDO also reflects the instability of eyeball rotations at the end of saccades. A previous computational modeling study also argued that the SDO cannot be attributed to the biomechanical properties of the eye movement mechanisms but was caused by the variation in neural control of saccades (Bahill et al., 1975aBahill A.T. Clark M.R. Stark L. Computer simulation of overshoot in saccadic eye movements.Comput. Programs Biomed. 1975; 4: 230-236Abstract Full Text PDF PubMed Scopus (11) Google Scholar). The frequency of SDO is quite capricious in individual subjects, i.e., SDO can occur on one day but is almost absent on another day (Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar). The reported frequency of SDO varies from 5% to 70% depending on the subject and experimental setup (Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar; Kapoula et al., 1986Kapoula Z.A. Robinson D.A. Hain T.C. Motion of the eye immediately after a saccade.Exp. Brain Res. 1986; 61: 386-394Crossref PubMed Scopus (78) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Lehman and Stark, 1983Lehman S.L. Stark L.W. Multipulse controller signals.3. Dynamic Overshoot.Biol. Cybern. 1983; 48: 9-10Crossref Scopus (5) Google Scholar). Reports have indicated that the frequency and amplitude of SDO in an individual subject are positively correlated with the velocity and deceleration of main saccades, i.e., a higher velocity and deceleration in main saccades corresponds to a greater number and amplitude of SDO (Hooge et al., 2015Hooge I. Nystrom M. Cornelissen T. Holmqvist K. The art of braking: post saccadic oscillations in the eye tracker signal decrease with increasing saccade size.Vis. Res. 2015; 112: 55-67Crossref PubMed Scopus (29) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar). However, controversial findings have also been reported (Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar; Fuchs, 1967Fuchs A.F. Saccadic and smooth pursuit eye movements in the monkey.J. Physiol. 1967; 191: 609-631Crossref PubMed Scopus (237) Google Scholar; Kimmel et al., 2012Kimmel D.L. Mammo D. Newsome W.T. Tracking the eye non-invasively: simultaneous comparison of the scleral search coil and optical tracking techniques in the macaque monkey.Front Behav. Neurosci. 2012; 6: 49Crossref PubMed Scopus (76) Google Scholar) (Hooge et al., 2015Hooge I. Nystrom M. Cornelissen T. Holmqvist K. The art of braking: post saccadic oscillations in the eye tracker signal decrease with increasing saccade size.Vis. Res. 2015; 112: 55-67Crossref PubMed Scopus (29) Google Scholar; Kapoula et al., 1986Kapoula Z.A. Robinson D.A. Hain T.C. Motion of the eye immediately after a saccade.Exp. Brain Res. 1986; 61: 386-394Crossref PubMed Scopus (78) Google Scholar; Van Gisbergen et al., 1981Van Gisbergen J.A. Robinson D.A. Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons.J. Neurophysiol. 1981; 45: 417-442Crossref PubMed Scopus (455) Google Scholar). So, the first goal of the present study is to determine the parameters of main saccade that are highly correlated with the occurrence of SDO, which will help to address the inconsistent and controversial findings among previous studies and to understand the possible mechanisms underlying SDO generation. Based on the common knowledge that it is more difficult to steadily stop a fast-moving object, we hypothesize that saccades with higher peak velocity and deceleration are more likely to have SDO. If our hypothesis is true, the occurrence of SDO should be different between young and elderly subjects, because the peak velocity of saccades is different between them (Dowiasch et al., 2015Dowiasch S. Marx S. Einhauser W. Bremmer F. Effects of aging on eye movements in the real world.Front Hum. Neurosci. 2015; 9: 46Crossref PubMed Scopus (85) Google Scholar; Irving et al., 2006Irving E.L. Steinbach M.J. Lillakas L. Babu R.J. Hutchings N. Horizontal saccade dynamics across the human life span.Invest Ophthalmol. Vis. Sci. 2006; 47: 2478-2484Crossref PubMed Scopus (153) Google Scholar; Sharpe and Zackon, 1987Sharpe J.A. Zackon D.H. Senescent saccades. Effects of aging on their accuracy, latency and velocity.Acta Otolaryngol. 1987; 104: 422-428Crossref PubMed Scopus (95) Google Scholar; Spooner et al., 1980Spooner J.W. Sakala S.M. Baloh R.W. Effect of aging on eye tracking.Arch. Neurol. 1980; 37: 575-576Crossref PubMed Scopus (161) Google Scholar; Warabi et al., 1984Warabi T. Kase M. Kato T. Effect of aging on the accuracy of visually guided saccadic eye movement.Ann. Neurol. 1984; 16: 449-454Crossref PubMed Scopus (103) Google Scholar). Indeed, previous studies have found that the amplitude of SDO was correlated with the subjects' age, but these studies showed opposite results. One paper illustrated that the amplitude of SDO increased in elderly subjects (Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar), whereas another paper showed that the amplitude of SDO decreased in elderly subjects (Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar). The second goal of the present study is to approach the aging effect on SDO. Several studies note that saccadic accuracy relies highly on the function of lower oculomotor structures (saccadic generator) in the brainstem and cerebellum (Optican and Pretegiani, 2017Optican L.M. Pretegiani E. What stops a saccade?.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017; 372: 20160194Crossref PubMed Scopus (23) Google Scholar; Van Gisbergen et al., 1981Van Gisbergen J.A. Robinson D.A. Gielen S. A quantitative analysis of generation of saccadic eye movements by burst neurons.J. Neurophysiol. 1981; 45: 417-442Crossref PubMed Scopus (455) Google Scholar; Zee and Robinson, 1979Zee D.S. Robinson D.A. A hypothetical explanation of saccadic oscillations.Ann. Neurol. 1979; 5: 405-414Crossref PubMed Scopus (231) Google Scholar); so far researches on the neural mechanisms underlying SDO have mainly focused on investigating the role of these oculomotor structures (Bahill et al., 1975aBahill A.T. Clark M.R. Stark L. Computer simulation of overshoot in saccadic eye movements.Comput. Programs Biomed. 1975; 4: 230-236Abstract Full Text PDF PubMed Scopus (11) Google Scholar, Bahill et al., 1975bBahill A.T. Clark M.R. Stark L. Dynamic overshoot in saccadic eye movements is caused by neurological control signed reversals.Exp. Neurol. 1975; 48: 107-122Crossref PubMed Scopus (140) Google Scholar; Ramat et al., 2005Ramat S. Leigh R.J. Zee D.S. Optican L.M. Ocular oscillations generated by coupling of brainstem excitatory and inhibitory saccadic burst neurons.Exp. Brain Res. 2005; 160: 89-106Crossref PubMed Scopus (86) Google Scholar; Ramat et al., 2008Ramat S. Leigh R.J. Zee D.S. Shaikh A.G. Optican L.M. Applying saccade models to account for oscillations.Prog. Brain Res. 2008; 171: 123-130Crossref PubMed Scopus (22) Google Scholar; Shaikh et al., 2008Shaikh A.G. Ramat S. Optican L.M. Miura K. Leigh R.J. Zee D.S. Saccadic burst cell membrane dysfunction is responsible for saccadic oscillations.J. Neuroophthalmol. 2008; 28: 329-336Crossref PubMed Scopus (57) Google Scholar). As we know, there are other oculomotor structures in the brain, e.g., the cerebral cortex, basal ganglia, and superior colliculus, which play important roles in the control of saccades. However, the effects of these higher oculomotor structures on SDO have not been explored. Therefore, the third goal of the present study is to assess the role of higher oculomotor structures in the development of SDO. Our hypothesis is that, if the higher oculomotor structures have the function to develop SDO as the lower oculomotor structures do, the specific changes in the spatiotemporal properties of SDO are expected to be seen in patients with PD and MCI compared with elderly healthy subjects. Otherwise, if the higher oculomotor structures just serve as a modulator to affect SDO through modulating the activity of lower oculomotor structures, there are no specific changes of SDO in patients with PD and MCI compared with elderly healthy subjects. In the present study, we analyzed the spatiotemporal characteristics of SDO in four groups of human subjects, namely, young healthy subjects, elderly healthy subjects, and patients with PD and MCI and in three saccadic tasks, i.e., visually guided step saccade, anti-saccade, and memory-guided saccade tasks (Figure S1). According to our data analysis criteria, we found two types of SDOs that show varied spatiotemporal properties: the simple saccadic dynamic overshoot (SDOsimple) with one backward small saccade immediately following the main saccade and the complex saccadic dynamic overshoot (SDOcomplex) with one backward and one forward small saccade immediately following the main saccade (Figure S2). We intend to address the following questions: (1) what parameters of the main saccade are highly correlated with the occurrence of SDO? (2) what is the effect of aging on SDO? (3) would the impairments of oculomotor structures in PD and MCI cause the specific changes of SDO? SDOs were identified as saccadic eye movements in our analysis (see methods for details). We analyzed the correlation between saccadic amplitude and peak velocity of all main saccades and their adhered SDOs, i.e., the saccadic main sequence analysis. We performed the linear regression on the log-transformed values of saccadic amplitude and peak velocity for each individual subject. The result of an example subject is plotted in Figure 1, which shows that the majority of data points, including the main saccades, SDO backward saccades, and SDO forward saccades, are linearly distributed in the log-log scale (linear regression, r2=0.909, p ≪ 0.001). Indeed, all subjects have such linear correlation between saccadic amplitude and peak velocity in the log-log scale (r2=0.911 on average, with a standard deviation of 0.081). These results indicate that the SDOs are indeed small saccadic eye movements. The effect of aging on the frequency and amplitude of SDO was disputed among previous studies (Deubel and Bridgeman, 1995aDeubel H. Bridgeman B. Fourth Purkinje image signals reveal eye-lens deviations and retinal image distortions during saccades.Vis. Res. 1995; 35: 529-538Crossref PubMed Scopus (101) Google Scholar; Mardanbegi et al., 2018Mardanbegi D. Killick R. Xia B. Wilcockson T. Gellersen H. Sawyer P. Crawford T.J. Effect of aging on post-saccadic oscillations.Vis. Res. 2018; 143: 1-8Crossref PubMed Scopus (8) Google Scholar). In addition, whether and how neurodegenerative diseases, such as PD and MCI, cause specific changes in the frequency and amplitude of SDO are unknown. To approach these questions, we calculate the fractions of SDO for each subject in each task and compare them among the four different groups of subjects. As shown in Figure 2A, the three groups of elderly subjects had a greater fraction of SDO than the young subjects in all three tasks. The difference is significant in the anti-saccade and memory-guided saccade tasks (Kruskal-Wallis test, anti-saccade, p < 0.001; memory-guided saccade, p < 0.001, Bonferroni correction, alpha = 0.05/6), although it does not reach the significant level in the visually guided step saccade task (Kruskal-Wallis test, p = 0.074). However, significant differences were not observed among the three groups of elderly subjects in any task (Tukey-Kramer multiple comparison test, all p values > 0.900). Furthermore, we also calculated the fraction of SDOcomplex over all SDOs. The results show that the average fractions of SDOcomplex in the young subjects were significantly lower than those in the elderly subjects (by over 20%) in all three tasks (Figure 2B; Kruskal-Wallis test, visually guided step saccade, p = 0.004; anti-saccade, p < 0.001; memory-guided saccade, p = 0.002, Bonferroni correction, alpha = 0.05/6). However, there were no significant differences among the three elderly groups in any task (Tukey-Kramer multiple comparison test, all p values > 0.541). Such results indicate that, although young subjects have a considerable fraction of saccades with SDOs, the majority of SDOs are the simple type, whereas elderly subjects have a greater fraction of saccades with SDOs than young subjects and approximately half of the SDOs are the complex type. We also compared the amplitude of the first return phase of SDOs (amplitude of SDO) among the four groups of subjects (Figure 2C). Overall, the average amplitude of SDO is smaller in the young subjects than in the elderly subjects in all three tasks. In particular, the difference is significant in both anti-saccades and memory-guided saccades (Kruskal-Wallis test, p = 0.018 and p = 0.005, respectively, Bonferroni correction, alpha = 0.05/6), although it does not reach significant level in the visually guided step saccade task (Kruskal-Wallis test, p = 0.177). Again, significant differences were not observed among the three groups of elderly subjects in any task (Tukey-Kramer multiple comparison test, all p values > 0.10). The relationship between the frequency/amplitude of SDO and the amplitude of the main saccades is controversial among previous studies. Here, we group the main saccades into three subsets based on the saccadic amplitude (2–6°, 6–9°, and 9–12°). For each individual subject, the required minimum trial number in each subset is five. Our data show that, in the young subjects, the frequency (Figure 3A) and amplitude (Figure 3B) of SDO are greater in saccades with larger amplitudes (>9°) than in saccades with smaller amplitudes (<9°) (Kruskal-Wallis test with Tukey-Kramer multiple comparison test, frequency: visually guided step saccade, p = 0.010; anti-saccade, p = 0.009; memory-guided saccade, p = 0.007; amplitude: visually guided step saccade, p = 0.032; anti-saccade, p = 0.079; memory-guided saccade, p = 0.012, Bonferroni correction, alpha = 0.05/3). In contrast, significant differences were not observed in the three groups of elderly subjects (all p values > 0.152) (Figures 3A and 3B). Such results show that, in elderly subjects, the amplitude of the main saccade is not closely correlated with the occurrence of SDO. If saccadic amplitude is not highly correlated with the frequency of SDO in elderly subjects, what factors might be? An intuitive thought is that, among saccades with similar amplitude, some of them with SDO might have higher velocity and/or deceleration, because in this case it is more difficult to brake the eye at the end of a saccade. To examine this speculation, both peak velocity and deceleration of main saccades were compared among the four groups of subjects based on the SDO characteristics (SDOwithout, SDOsi" @default.
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