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      The influence of stimulus and behavioral histories on predictive control of smooth pursuit eye movements

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          Abstract

          The smooth pursuit system has the ability to perform predictive feedforward control of eye movements. This study attempted to examine how stimulus and behavioral histories of past trials affect the control of predictive pursuit of target motion with randomized velocities. We used sequential ramp stimuli where the rightward velocity was fixed at 16 deg/s while the leftward velocity was either fixed (predictable) at one of seven velocities (4, 8, 12, 16, 20, 24, or 28 deg/s) or randomized (unpredictable). As a result, predictive pursuit responses were observed not only in the predictable condition but also in the unpredictable condition. Linear mixed-effects (LME) models showed that both stimulus and behavioral histories of the previous two or three trials influenced the predictive pursuit responses in the unpredictable condition. Intriguingly, the goodness of fit of the LME model was improved when both historical effects were fitted simultaneously rather than when each type of historical data was fitted alone. Our results suggest that predictive pursuit systems allow us to track randomized target motion using weighted averaging of the information of target velocity (stimulus) and motor output (behavior) in past time sequences.

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          Cognitive processes involved in smooth pursuit eye movements.

          Ocular pursuit movements allow moving objects to be tracked with a combination of smooth movements and saccades. The principal objective is to maintain smooth eye velocity close to object velocity, thus minimising retinal image motion and maintaining acuity. Saccadic movements serve to realign the image if it falls outside the fovea, the area of highest acuity. Pursuit movements are often portrayed as voluntary but their basis lies in processes that sense retinal motion and can induce eye movements without active participation. The factor distinguishing pursuit from such reflexive movements is the ability to select and track a single object when presented with multiple stimuli. The selective process requires attention, which appears to raise the gain for the selected object and/or suppress that associated with other stimuli, the resulting competition often reducing pursuit velocity. Although pursuit is essentially a feedback process, delays in motion processing create problems of stability and speed of response. This is countered by predictive processes, probably operating through internal efference copy (extra-retinal) mechanisms using short-term memory to store velocity and timing information from prior stimulation. In response to constant velocity motion, the initial response is visually driven, but extra-retinal mechanisms rapidly take over and sustain pursuit. The same extra-retinal mechanisms may also be responsible for generating anticipatory smooth pursuit movements when past experience creates expectancy of impending object motion. Similar, but more complex, processes appear to operate during periodic pursuit, where partial trajectory information is stored and released in anticipation of expected future motion, thus minimising phase errors associated with motion processing delays.
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            Calculating correlation coefficients with repeated observations: Part 1--Correlation within subjects.

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              Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence.

              1. The introduction of a period of darkness between the disappearance of an initial fixation target and the appearance of a peripheral saccade target produces a general reduction in saccadic reaction time (SRT)-known as the gap effect- and often very short latency express saccades. To account for these phenomena, premotor processes may be facilitated by release of visual fixation and advanced preparation of saccadic programs. The experiments described in this paper were designed to test the relevance of the ocular fixation disengagement and oculomotor preparation hypotheses by identifying the influence of different factors on SRTs and the occurrence of express saccades in the monkey. 2. The SRTs of two monkeys were measured in two behavioral paradigms. A peripheral saccade target appeared at the time of disappearance of a central fixation target in the no-gap task, whereas a 200-ms period of no stimuli was interposed between the fixation target disappearance and the saccade target appearance in the gap task. The distribution of SRTs in these tasks was generally bimodal; the first and second mode was composed of express and regular saccades, respectively. We measured the mean SRT, mean regular saccade latency, mean express saccade latency, and percentage of express saccades in both tasks. We also estimated the gap effect, i.e., the difference between the SRTs in no-gap trial and the SRTs in gap trials. 3. Once the animals were trained to make saccades to a single target location and produce express saccades, SRTs in both no-gap and gap trials displayed a broad tuning with respect to the spatial location of the trained target when the target location was varied randomly in a block of trials. Express saccades were made only to a restricted region of the visual field surrounding the trained target location. A gap effect was present for nearly all target locations tested, irrespective of express saccade occurrence. Finally, the probability of generating an express saccade at the trained target location decreased with the introduction of uncertainty about target location. 4. The occurrence of express saccades increased with the duration of the visual and nonvisual (gap) fixation that the animal was required to maintain before the onset of a saccade target. The gap duration was effective in reducing the mean SRT for gaps < or = 300 ms, and it was more influential than comparable variation in the visual fixation duration. 5. The occurrence of express saccades made to targets of identical eccentricity increased when the initial eye fixation position was shifted eccentric in a direction opposite to the saccade direction. Concomitantly, mean SRT decreased by approximately 2 ms for each 1-deg change in initial eye fixation position. 6. The occurrence of express saccades depended upon contextual factors, i.e., on both the behavioral task (no-gap or gap) and the latency of the saccade that the monkey executed to the same target in the preceding trial. The highest percentage of express saccades was observed after an express saccade in a no-gap trial, whereas the lowest percentage was obtained after a regular saccade in a gap trial. 7. These findings indicate that training-dependent express saccades are restricted to a specific spatial location dictated by the training target, and their incidence is facilitated by high predictability of target presentation, long-duration foreperiod, absence of visual fixation, eccentric initial eye position opposite to the saccade direction, and express saccade occurrence in the previous trial. The release of fixation afforded by the gap accounts for the general gap effect, but has only a modulatory influence on express saccade generation. We conclude that advanced motor preparation of saccadic programs generally reduces SRT and is primarily responsible for the occurrence of express saccades, which therefore may be caused mainly by neuronal changes restricted to a specific locus-coding for the trained movemen
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                Author and article information

                Contributors
                ono.seiji.fp@u.tsukuba.ac.jp
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                16 November 2021
                16 November 2021
                2021
                : 11
                : 22327
                Affiliations
                [1 ]GRID grid.20515.33, ISNI 0000 0001 2369 4728, Faculty of Health and Sport Sciences, , University of Tsukuba, ; Ibaraki, Japan
                [2 ]GRID grid.254217.7, ISNI 0000 0000 8868 2202, Department of Robotic Science and Technology, , Chubu University College of Engineering, ; Kasugai, Japan
                [3 ]GRID grid.254217.7, ISNI 0000 0000 8868 2202, Center for Mathematical Science and Artificial Intelligence, , Chubu University, ; Kasugai, Japan
                [4 ]GRID grid.254217.7, ISNI 0000 0000 8868 2202, Academy of Emerging Sciences, , Chubu University, ; Kasugai, Japan
                [5 ]GRID grid.265061.6, ISNI 0000 0001 1516 6626, Department of Physiology, , Tokai University School of Medicine, ; Kanagawa, Japan
                [6 ]GRID grid.416859.7, ISNI 0000 0000 9832 2227, Department of Pathology of Mental Diseases, , National Institute of Mental Health, National Center of Neurology and Psychiatry, ; Tokyo, Japan
                [7 ]GRID grid.258799.8, ISNI 0000 0004 0372 2033, Graduate School of Medicine, , Kyoto University, ; Kyoto, Japan
                Article
                1733
                10.1038/s41598-021-01733-1
                8595731
                34785718
                dc4e37cb-7ee6-405a-a113-3705c8f252bf
                © The Author(s) 2021

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 21 June 2021
                : 2 November 2021
                Funding
                Funded by: University of Tsukuba Basic Research Support Program Type A
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 18KK0286
                Award ID: 18KK0286
                Award ID: 18KK0286
                Award ID: 18KK0286
                Award Recipient :
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                © The Author(s) 2021

                Uncategorized
                motor control,visual system
                Uncategorized
                motor control, visual system

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