A dynamic representation of target motion drives predictive smooth pursuit during target blanking. We tested human responses to high-frequency perturbations during step-ramp pursuit, as well as the pursuit of a periodically moving target. J. Neurosci. 248, 164189. https://doi.org/10.1113/jphysiol.1961.sp006811, https://doi.org/10.1016/0042-6989(84)90010-5, https://doi.org/10.1146/annurev.ne.10.030187.000525, https://doi.org/10.1016/0022-3956(88)90005-2, https://doi.org/10.1016/j.anl.2004.11.009, https://doi.org/10.1016/j.ejpn.2008.07.003, https://doi.org/10.1016/s0161-6420(80)35280-9, https://doi.org/10.1016/j.braindev.2005.03.005, https://doi.org/10.1371/journal.pone.0083972, https://ui.adsabs.harvard.edu/abs/2015arXiv151202325L, https://doi.org/10.1016/j.visres.2005.06.027, https://doi.org/10.1080/09273970601180289, http://creativecommons.org/licenses/by/4.0/. 1C of the target. Harley, R. D. Paralytic strabismus in children. What is SMOOTH-PURSUIT MOVEMENT? Barnes, G. R. (1993). conceived the project and designed the experiments. Lisberger, S. G. (1998). The Vestibular System. Rashbass, C. The relationship between saccadic and smooth tracking eye movements. Neurol. Click here . Vis. 60, 604620. This preparatory activity appears to be linked to anticipatory smooth pursuit, which is also dependent on stimulus predictability (Heinen et al., 2005; de Hemptinne et al., 2007, 2008). 259, 571590. Cheng, M., and Outerbridge, J. S. (1975). Saccades are detected using a velocity threshold; this is not reliable in general, because the velocity ranges of saccades and smooth pursuit overlap. 8, 6.113. Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys. Keywords: smooth pursuit, eye movements, anticipation, efference copy, species comparisons, prediction, computational modeling, pathophysiology, Citation: Fukushima K, Fukushima J, Warabi T and Barnes GR (2013) Cognitive processes involved in smooth pursuit eye movements: behavioral evidence, neural substrate and clinical correlation. Model of ocular pursuit. Analysis of smooth pursuit eye movements in a clinical context by tracking the target and eyes. Responses of visual-tracking neurons from cortical area MST-l to visual, eye and head motion. Brain Res. In the initial 2030 ms eye acceleration shows some increase with target velocity but not with starting position of the target motion (Lisberger and Westbrook, 1985; Tychsen and Lisberger, 1986), whereas, in the period 6080 ms after onset there is a much greater modulation of eye acceleration by target velocity and a strong dependence on eccentricity of starting position. Neuroreport 12, 14091414. (2008). It is possible, therefore, that this summation may take place further downstream in, for example, the vestibular nuclei. Figure 12. Crucially, PD patients may not be capable of this modification of wT1 since their responses in the memory pursuit task do not show an abrupt increase in acceleration (Ito et al., 2012), even with a popout stimulus (Figure 13D). CAS The influence of display characteristics on active pursuit and passively induced eye movements. Aim Deficits in smooth-pursuit eye movements (SPEM) are often associated with mild traumatic brain injury (TBI). Then, the eye position data at 240Hz were synchronized with the target data at 29.97Hz. 59, 548558. We analyze the smooth components of the eye movements separately from the saccades. Later (typically after a year of training), saccade latency to spot motion shortened usually to about 220 ms, and preceding the saccades, initial smooth-pursuit appeared with latencies typically of 130150 ms (Figure 6B2, arrow). Brain Res. Mahaffy and Krauzlis (2011) reported that inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection, consistent with our muscimol inactivation of the caudal FEF (Fukushima et al., 2011b). 13, 87100. The 25th and 75th percentile points of the maximum values in the centrifugal direction were explored (the green horizontal lines). With prolonged stimulation eye velocity settles to an average that is close to target velocity. 14, 225232. Their activity was not modulated during sinusoidal pursuit using a single spot, suggesting that it was unrelated to eye movement per se. The smooth pursuit system incorporates closed-loop neuronal systems, continuously utilizing real-time negative feedback, for the critical task of maintaining optimal fixation of a target in motion by aligning it with the fovea ( 19 ). 53, 325336. A. Heinen, S. J., Badler, J. Cerebellum 2, 223232. Predictive signals in the pursuit area of the monkey frontal eye fields. (2009). and more. 148, 350365. Vision Res. Goldberg, J. M., Wilson, V. J., Cullen, K. E., Angelaki, D. E., Broussard, D. M., Bttner-Ennever, J. Voluntary selection of the target for smooth eye movement in the presence of superimposed, full-field stationary and moving stimuli. Effects of an optokinetic background on pursuit eye movements. 64, 191201. CAS Human smooth pursuit: stimulus-dependent responses. Smooth-pursuit eye movements allow primates to track moving objects. Ex: Reading a road sign while driving 2) Cancellation of VOR during head tracking. Westheimer, B., and Blair, M. (1973). Abnormalities of smooth pursuit eye movement (SPEM) are a clinical finding in central equilibrium disorders. Cereb. Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements. Detailed examination of the step-ramp response has shown two distinct phases. Lisberger, S. G., Morris, E. J. Article Signals similar to those seen in the SEF and caudal FEF were also represented in the oculomotor vermis/caudal fastigial nucleus and the floccular region, although clear differences were also observed (Fukushima et al., 2011c). Visual motion processing and sensory-motor integration for smooth pursuit eye movements. 115, 12201227. DISCUSSION In a peripheral vestibular lesion, strong spontaneous nystagmus can produce abnormalities of pendular eye movement [3]. The data that support the findings of this study are openly available in Zenodo (https://doi.org/10.5281/zenodo.6400751). See text for further explanation. 129, 5767. 7:4. doi: 10.3389/fnsys.2013.00004. The present article shows that using binocular information for discrimination of fixations and smooth pursuit movements is advantageous in static stimuli, without impairing the algorithm's ability to detect smoother pursuit movements in video and moving-dot stimuli. (B) Memory-based pursuit when cue 1 visual motion was leftward and cue 2 instruction was go. Progressive bradykinesia and hypokinesia of ocular pursuit in Parkinson's disease. Eye velocity trajectories during target extinction. As illustrated in Figure 6B1, the monkey initiated the final action by saccades (but not by smooth-pursuit) with latencies typically 260300 ms (B1, upward arrow), and these saccades were followed by smooth-pursuit. Brain Res. The dorsolateral prefrontal cortex has been linked to temporal storage of sensory signals (i.e., working memory, Goldman-Rakic, 1995). Brain Res. Models based on control theory have been used very successfully to describe the dynamic characteristics of pursuit (Robinson et al., 1986). Sheliga, B. M., Riggio, L., and Rizzolatti, G. (1994). (1) Discharge characteristics of no-go neurons in all these areas were basically similar (Figures 10B,E), but mean latencies (re cue 2 onset) of no-go responses in the oculomotor vermis/cFN were significantly longer (>250 ms, p < 0.001) than those of SEF/caudal FEF no-go neurons (Fukushima et al., 2011c). Ferrera and Lisberger (1995, 1997) showed that the initial open-loop response is a vector average of the responses that would be made to individual stimuli. Characteristic of Parkinson's disease (PD) are difficulties in initiating volitional movements and, when initiated, slow and hypo-metric movement (e.g., Warabi et al., 2011). Opin. Smooth pursuit tracking is susceptible to an age-effect and may require that the examiner acclimate the patient to the task prior to recording. Raising gain in the indirect pathway (wT1) is the primary factor responsible for the initial high acceleration pursuit response, the extra-retinal component giving a lower level of eye acceleration and developing later than the visually driven component (see Figure 4D). Lee, E. Y., Cowan, N., Vogel, E. K., Rolan, T., Valle-Inclan, F., and Hackley, S. A. Figure8 shows the patients horizontal and vertical eye movements. The target location and both eye positions at the peak time were defined as maximum values. Cereb. Efficient pursuit requires appropriate target selection and predictive compensation for inherent processing delays. We show how neuronal activity may be explained by models of retinal and extra-retinal interaction in target selection and predictive control and thus aid understanding of underlying pathophysiology. Smooth pursuit movements are much slower tracking movements of the eyes designed to keep a moving stimulus on the fovea. As shown in Figure 4A, because the initial visually-driven components of Mid-ramp and Short-ramp responses were very similar, their effect was eliminated, revealing that the difference signal increased with time with much lower acceleration than the visually-driven component. The measurement error (interquartile range) was 0.20.5 at a distance of 1.0m. The scene camera recorded the real scenes (resolution, 640480 pixels; angle of view,31 from the center of the scene camera) with a sampling rate of 29.97Hz. Clin. (B) Time course of mean (SE) discharge of the 24 no-go SEF neurons during no-go (red) and go (black) trials. The simplest way to assess pursuit performance is to examine the response to the sudden onset of an unexpected, constant velocity target motion (a ramp stimulus). J. Neurophysiol. This fits with an important observation, that during pursuit of a target that unexpectedly disappears, smooth eye movements do not simply stop but can be sustained, albeit at reduced velocity, in both humans (Von Noorden and Mackensen, 1962; Becker and Fuchs, 1985) and monkeys (Newsome et al., 1988). Invest. From there, output signals are sent in two directions; one to pontine nuclei, primarily to the dorso-lateral pontine nuclei (DLPN), and through the cerebellar floccular region that includes the flocculus and ventral paraflocculus (Gerrits and Voogd, 1989), signals are sent to vestibular nuclei. In dierent experiments, we record subjects' eye movements in response to dierent types of stimuli. Noda, H., Sugita, S., and Ikeda, Y. Schlindwein, P., Mueller, M., Bauermann, T., Brandt, T., Stoeter, P., and Dieterich, M. (2008). Deno, D. C., Crandall, W. F., Sherman, K., and Keller, E. L. (1995). and transmitted securely. (2002). Ophthalmology 87, 2443. The median of the target location was calculated both horizontally and vertically, respectively, and was defined as the relative origin (C). 1233, 117126. Smooth Pursuit Pursuit is a voluntary response, controlled by attention to moving objects. Fukushima, K. (2003a). Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. Lett. Cortex 21, 19101924. Pursuit . 46, 163170. ], and 19K21783 [Y.I. Vision Res. https://doi.org/10.1136/jnnp.56.7.799 (1993). Popout enhances and advances target selection. Velocity profile of smooth pursuit eye movements in humans: pursuit velocity increase linked with the initial saccade occurrence. Neuron 14, 477485. N.Y. Acad. Syst. 140, 239254. Pos and vel indicate position and velocity. Google Scholar. Pursuit movement is the ability of the eyes to smoothly follow a moving object. Lett. Science 190, 906908. Ann N Y Acad Sci. Bennett, S. J., and Barnes, G. R. (2003). In particular, caudal FEF inactivation not only decreased eye velocity gain, but impaired delay compensation of pursuit eye movements during sinusoidal pursuit of a singe spot at frequencies ~1 Hz, suggesting that the caudal FEF is necessary for response delay compensation during sinusoidal pursuit. The lack of initial pursuit and deficient postsaccadic enhancement in most PD patients are unlikely to be due to impairments of smooth-pursuit eye movements per se, since during simple ramp pursuit of a single spot moving at the same velocity, the same patients clearly exhibited an initial pursuit component before saccades, similar to normal controls (Figures 11A2 vs. B2 *), and since postsaccadic enhancement of smooth-pursuit was also seen at least for the first saccades after spot motion (A2 and B2, downward arrows). Barnes, G. R., and Asselman, P. T. (1992). (F) Superimposition of the relative origin data, which is the same as Fig. Figure 8B plots a difference in time course of mean discharge of visual memory neurons (red) and visual memory + movement-preparation neurons (blue) in the SEF during go trials in their preferred directions. U.S.A. 108, 1606816073. Single-unit task-related neuronal activity was examined in medial superior temporal cortex (MST), supplementary eye fields (SEF), caudal frontal eye fields (FEF), cerebellar dorsal vermis lobules VIVII, caudal fastigial nuclei (cFN), and floccular region. Accordingly, electrical stimulation in the region of OPNs inhibits premotor neurons and interrupts saccades. The gains in all directions were not significantly different between left (0.9360.186 in all directions) and right (0.9160.180 in all directions) eyes (P>0.52, Wilcoxon signed-rank test with Bonferroni correction; Fig. There was no significant difference in the percent of movement-preparation neurons (Figure 9A, delay 2) between the two areas. Boman, D. K., and Hotson, J. R. (1988). 57, 17571764. Collins, C. J. S., and Barnes, G. R. (2005). Neuronal activity reflecting working memory of visual motion direction and go/no-go selection was found predominantly in SEF, cerebellar dorsal vermis and cFN, whereas movement preparation related signals were found predominantly in caudal FEF and the same cerebellar areas. Heuer, H. W., and Britten, K. H. (2004). On average, activity was reduced by 34% but never completely stopped or paused. PubMed For this, the stationary spot remained centered, but spawned two identical spots; one that moved in the direction instructed by cue 1 and the other moved in the opposite direction at 10/s. An important generic feature of these models is that if visual feedback is suddenly cut off, the efference copy feedback loop can sustain the response to some extent (Figure 1C). Vision Res. (1975). Comparison of visual latencies of neurons that exhibited directional visual motion responses to cue 1 indicates that neurons with shorter visual latencies were significantly more frequent in the caudal FEF than the SEF (Figure 9B, Fukushima et al., 2011b). Vision Res. Exp. Figure 2. 4, 539553. Our hypothesis is that active pursuit of a single target in the simple ramp task is achieved by augmentation of gain for the selected target by increasing open-loop gain (wT1) in the indirect pathway and concomitantly initiating extra-retinal activity in the efference copy loop (i.e., increasing 1). Bookshelf 18, 537539. Parameter values (see Figure 2): Te = 0.12 s; = 1; K0 = 3 (right); K0 = 2 (left). https://doi.org/10.1016/j.ejpn.2008.07.003 (2009). 27, 10121018. This task differed from the foveofugal step-ramp paradigm in that the target began moving smoothly from the centre without first stepping abruptly from the centre. Eye velocity (vel) during saccades was clipped. Derivation of retinal and extra-retinal pursuit components. (2009) and Fukushima et al. J. Neurophysiol. (B) Comparison of latencies of visual motion responses of caudal FEF and SEF neurons to cue 1. (2011). Ackerley, R., and Barnes, G. R. (2011). (2012). 2011. No-go neurons are also different from fixation neurons in the FEF (Izawa et al., 2009, 2011), since no-go neurons in the memory-based pursuit/saccade task exhibited significant discharge only after cue 2 but not before (e.g., during cue 1 or delay 1), despite that the monkeys fixated a stationary spot during these periods (Figures 10AE). But unlike PD patients (e.g., Figure 11A2), corrective saccades of the cerebellar patient were followed by centripetal drift due to neural integrator failure, resulting in little pursuit eye velocity (Figure 12A; also Westheimer and Blair, 1973, 1974). 7:5. doi: 10.1167/7.1.5. Orban de Xivry, J. J., Missal, M., and Lefvre, P. (2009). We analyzed the differences in the latencies and gains between both eyes in each direction using the Wilcoxon signed-rank test with Bonferroni correction used to adjust the P values. 28, 11571165. (2011c). Storage of timing information is an important aspect of other motor control processes (see Ivry and Spencer, 2004, for review). 63, 815831. (A) Eye velocity responses to left (negative) and right (positive) from a single monkey during simple ramp pursuit (SR) vs. memory pursuit (MP). Frontal cortical control of smooth-pursuit. Oscillatory eye movements resembling pendular nystagmus in normal juvenile macaques. e-mail: g.r.barnes@manchester.ac.uk, Eye movement-related brain activity during perceptual and cognitive processing, View all
Dysfunctional mode switching between fixation and saccades: collaborative insights into two unusual clinical disorders. Cite this article. 99, 831842. We plan to investigate the characteristics of eye movements in paralytic strabismus. Visual motion processing for the initiation of smooth-pursuit eye movements in humans. Sci. Open arrowheads with dashed lines in (B) schematically indicate a proposed smooth-pursuit efference copy loop between the caudal FEF and the basal ganglia through the thalamus which is not shown in (A) (adapted from Cui et al., 2003). Elife. These results suggest that PD patients with working memory impairment may have frontal cortical dysfunction that includes the SEF (e.g., Possin et al., 2008; Lee et al., 2010). Epub 2020 Sep 30. We evaluated the accuracy of the classification in each direction between the peak fittingbased and threshold-based detection using Fisher's exact test with the degree of feedom was set 1. Examples of reactive and anticipatory pursuit. Smooth-pursuit eye movements support scrutiny of objects moving in space by matching eye velocity to target velocity in order to both reduce retinal blur of the moving object and facilitate its continued foveation. Neurosci. 10, 97129. Simple ramp and memory-based pursuit responses.
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