Predictive Smooth Ocular Pursuit During the Transient Disappearance of a Visual Target

The University of Manchester, Manchester, England, United Kingdom
Journal of Neurophysiology (Impact Factor: 2.89). 08/2004; 92(1):578-90. DOI: 10.1152/jn.01188.2003
Source: PubMed


When a moving target disappears and there is a complete absence of visual feedback signals, eye velocity decays rapidly but often recovers to previous levels if there is an expectation the target will reappear further along its trajectory Given that eye velocity cannot be maintained under such circumstances, the anticipatory recovery may function to minimize the developing velocity error. When there is a change in target velocity during a transient, any recovery should ideally be scaled and hence predictive of the expected target velocity at reappearance. This study confirmed that subjects did not maintain eye velocity close to target velocity for the duration of the inter-stimulus interval (ISI). The majority of subjects exhibited an initial reduction in eye velocity followed by a scaled recovery prior to target reappearance. Eye velocity during the ISI was, therefore, predictive of the expected change in target velocity. These behavioral data were simulated using a model in which gain applied to the visuomotor drive is reduced after the loss of visual feedback and then modulated depending on subject's expectation regarding the target's future trajectory.

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    • "In all cases, though, expectation is the critical factor that allows initiation of such internally generated movements (Kowler, 1989; Barnes et al., 2002). Expectation is also a critical factor in the maintenance of eye velocity during occlusion; without expectation of target reappearance, eye velocity rapidly declines toward zero (Mitrani and Dimitrov, 1978; Bennett and Barnes, 2004), even when the subject attempts to continue pursuit, as evidenced by the fairly successful ability to follow the future target movement (Figure 1D). "
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    ABSTRACT: Smooth-pursuit eye movements allow primates to track moving objects. Efficient pursuit requires appropriate target selection and predictive compensation for inherent processing delays. Prediction depends on expectation of future object motion, storage of motion information and use of extra-retinal mechanisms in addition to visual feedback. We present behavioural evidence of how cognitive processes are involved in predictive pursuit in normal humans and then describe neuronal responses in monkeys and behavioural responses in patients using a new technique to test these cognitive controls. The new technique examines the neural substrate of working memory and movement preparation for predictive pursuit by using a memory-based task in macaque monkeys trained to pursue (go) or not pursue (no-go) according to a go/no-go cue, in a direction based on memory of a previously presented visual motion display. 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 VI-VII, caudal fastigial nuclei (cFN), and floccular region. 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. Chemical inactivation produced effects consistent with differences in signals represented in each area. When applied to patients with Parkinson's disease, the task revealed deficits in movement preparation but not working memory. In contrast, patients with frontal cortical or cerebellar dysfunction had high error rates, suggesting impaired working memory. 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.
    Frontiers in Systems Neuroscience 03/2013; 7:4. DOI:10.3389/fnsys.2013.00004
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    • "Ongoing pursuit can be reasonably well maintained at a lower gain in the absence of a visual target. The predictive pursuit, predictive maintenance, and predictive recovery have been studied in experimental paradigms in which a moving target was transiently occluded (Becker and Fuchs 1985; Bennett and Barnes 2003–2006; Boman and Hotson 1992; Mrotek and Soechting 2007b; Orban de Xivry et al. 2006). It seems to rely on a combination of reflexive and voluntary control mechanisms. "
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    ABSTRACT: Success of motor behavior often depends on the ability to predict the path of moving objects. Here we asked whether tracking a visual object with smooth pursuit eye movements helps to predict its motion direction. We developed a paradigm, "eye soccer," in which observers had to either track or fixate a visual target (ball) and judge whether it would have hit or missed a stationary vertical line segment (goal). Ball and goal were presented briefly for 100-500 ms and disappeared from the screen together before the perceptual judgment was prompted. In pursuit conditions, the ball moved towards the goal; in fixation conditions, the goal moved towards the stationary ball, resulting in similar retinal stimulation during pursuit and fixation. We also tested the condition in which the goal was fixated and the ball moved. Motion direction prediction was significantly better in pursuit than in fixation trials, regardless of whether ball or goal served as fixation target. In both fixation and pursuit trials, prediction performance was better when eye movements were accurate. Performance also increased with shorter ball-goal distance and longer presentation duration. A longer trajectory did not affect performance. During pursuit, an efference copy signal might provide additional motion information, leading to the advantage in motion prediction.
    Journal of Neurophysiology 02/2011; 105(4):1756-67. DOI:10.1152/jn.00344.2010 · 2.89 Impact Factor
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    • "Head and gaze displacement signals were then digitally differentiated to obtain corresponding velocity signals. Before the main analysis, saccadic movements and blinks were removed using an interactive graphics procedure [see (Bennett et al. 2004)]. Linear interpolation was used to fill the gaps after saccade removal, and the resultant smooth gaze velocity movements were filtered with a 30-Hz zero-phase digital low-pass filter. "
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    ABSTRACT: We investigated how effectively briefly presented visual motion could be assimilated and used to track future target motion with head and eyes during target disappearance. Without vision, continuation of eye and head movement is controlled by internal (extra-retinal) mechanisms, but head movement stimulates compensatory vestibulo-ocular reflex (VOR) responses that must be countermanded for gaze to remain in the direction of target motion. We used target exposures of 50-200 ms at the start of randomised step-ramp stimuli, followed by > 400 ms of target disappearance, to investigate the ability to sample target velocity and subsequently generate internally controlled responses. Subjects could appropriately grade gaze velocity to different target velocities without visual feedback, but responses were fully developed only when exposure was > 100 ms. Gaze velocities were sustained or even increased during target disappearance, especially when there was expectation of target reappearance, but they were always less than for controls, where the target was continuously visible. Gaze velocity remained in the direction of target motion throughout target extinction, implying that compensatory (VOR) responses were suppressed by internal drive mechanisms. Regression analysis revealed that the underlying compensatory response remained active, but with gain slightly less than unity (0.85), resulting in head-free gaze responses that were very similar to, but slightly greater than, head-fixed. The sampled velocity information was also used to grade head velocity, but in contrast to gaze, head velocity was similar whether the target was briefly or continuously presented, suggesting that head motion was controlled by internal mechanisms alone, without direct influence of visual feedback.
    Experimental Brain Research 02/2011; 210(3-4):569-82. DOI:10.1007/s00221-011-2566-6 · 2.04 Impact Factor
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