Elsevier

Cognitive Brain Research

Volume 25, Issue 3, December 2005, Pages 688-700
Cognitive Brain Research

Research Report
Attention and selection for predictive smooth pursuit eye movements

https://doi.org/10.1016/j.cogbrainres.2005.08.016Get rights and content

Abstract

Humans cannot typically produce smooth eye movements in the absence of a moving stimulus. However, they can produce predictive smooth eye movements if they expect a target of a known velocity to reappear. Here, we observed that participants could extract velocity information from two simultaneously presented moving targets in order to produce a subsequent predictive smooth eye movement for one of the two targets. Subjects fixated a stationary cross during the presentation of two targets, moving rightward at different velocities. In the next presentation, a single target was presented, which participants tracked with their eyes. A static cue, presented 700 ms before the moving target, indicated which of the two targets would be presented. Predictive eye movements were of an appropriate velocity, even when participants did not know in advance which of the two targets would subsequently be cued. However, the scaling of predictive eye velocity was marginally less accurate in this divided attention condition than when participants knew the identity of the cued target in advance, or a single target was presented during fixation. In a second experiment, we found that the velocity cued on the previous trial had a greater effect than the uncued velocity on the current trial. The negligible effect of the uncued velocity indicates that participants were extremely effective at selectively reproducing one of two recently viewed velocities. However, other influences, such as past history, also affected predictive smooth eye movements.

Introduction

Humans typically cannot produce smooth eye movements without a moving target to follow. However, if a moving stimulus is presented repeatedly, humans are able to make predictive eye movements, i.e., begin to move their eyes at an appropriate velocity prior to the appearance of the moving target [5]. Indeed, humans are able to make predictive eye movements even if they fixated during the initial presentation and did not actively follow the moving target [7]. This has been attributed to a short-term velocity store [48]. In the current work, we investigated a more complex situation in which two moving targets are presented.

Many authors have emphasized the role of selection and attention in smooth pursuit [3], [4], [22], [29], [31], [35]. For example, Atkin [1] states that “…conflicting and redundant velocity information available to the pursuit control system can be utilized in a highly selective manner,” and it has been demonstrated that participants can track a moving target against stationary and moving backgrounds [29], [50]. More recent studies of elicited smooth pursuit in both humans and monkeys have shown that participants can selectively track one of two moving objects, when the selected object is either cued by the experimenter [15], [16], [32] or chosen by the participant [33]. In the latter case, monkeys typically make an initial eye movement that is the average of the two target directions, before making a saccade to one or other target, and exhibiting the velocity of the selected target post-saccade [17]. Furthermore, it was recently shown that when a saccade was produced by microstimulation which brought the monkey's eye to one of two moving targets, the monkey took on the velocity of the target at the end point of this evoked saccade [18]. This suggests that the velocities of both targets were represented prior to a decision being made about which target to follow [43].

Previous studies of selection and smooth pursuit have investigated how people select which object to track, from simultaneously presented moving objects. Here, we investigated the selective reproduction of previously viewed velocities. In an initial study, we developed a task in which participants fixated during the presentation of two targets moving at different velocities, before tracking one of the targets during a subsequent presentation (Fig. 1; [36]). We demonstrated that participants were able to make a predictive eye movement of an appropriate velocity, for one of two previously viewed targets. They were able to do so, despite being uncertain which of the two targets they would subsequently be required to follow. These results indicate that participants were able to exert cognitive control and select which previously viewed velocity to reproduce. Hereafter, the velocity of the target presented in the tracking presentation is referred to as the cued velocity, and the velocity of the target presented only during fixation is referred to as the uncued velocity.

This initial study threw up several questions. How does performance with two targets compare to performance with a single target? In other words, is there a cost to the dividing of resources between the 2 targets (henceforth referred to as the Divided condition)? And would there be any benefit in knowing the identity of the cued target in advance? Research into motion perception has shown that people can selectively attend to motion [10] or a particular direction of motion [2], [39], [44]. Third, what are the effects of the uncued velocity, i.e., the velocity of the target which is viewed but never tracked? In Experiment 1 of the current study, we compared the Divided condition to a Selective condition, in which the same target (upper or lower) was cued throughout a block. Both these conditions were compared to a control Single condition in which a single target was presented during fixation. In Experiment 2, we explored competing influences on the predictive eye movement in a particular trial, by systematically investigating the effects of the uncued velocity, the previously cued velocity and the previously uncued velocity.

Section snippets

Experiment 1

Each trial of the task involved 2 presentations: participants fixated during an initial presentation of moving stimuli and then tracked a single moving target on the next presentation. In the Divided condition, 2 targets were presented in the fixation condition, and a cue was presented before the tracking presentation to indicate which target they would be required to follow. In the Selective condition, the stimuli were the same as the Divided condition, but the same target was cued throughout

Experiment 2

There were two main aims of this experiment. First, to examine the effects of cued and uncued velocity in the Divided condition controlling for previously cued velocity and for switching between targets. Second, to directly examine the effect of the cued or uncued velocities presented in the previous trial and whether this effect is modulated by switching or remaining tracking the same target. This was accomplished using an interleaved trial design and only Divided and Single conditions; the

General discussion

We have demonstrated that participants are able to extract velocity information from two simultaneously moving targets and produce a subsequent predictive eye movement for just one of these targets (see also [36]). In the current study, the target always moved in a rightward direction, but we can conclude that the eye movements were predictive as they were at an appropriate velocity for the cued target; if participants were making a generic rightward movement, eye velocity would be at an

References (50)

  • B.J. Scholl

    Objects and attention: the state of the art

    Cognition

    (2001)
  • B.J. Scholl et al.

    Tracking multiple items through occlusion: clues to visual objecthood

    Cogn. Psychol.

    (1999)
  • A. Atkin

    Selection of sensory information in control of pursuit eye movements

    Psychonom. Sci.

    (1967)
  • K. Ball et al.

    Cues reduce direction uncertainty and enhance motion detection

    Percept. Psychophys.

    (1981)
  • G.R. Barnes et al.

    The interaction of conflicting retinal motion stimuli in oculomotor control

    Exp. Brain Res.

    (1985)
  • G.R. Barnes et al.

    The remembered pursuit task: evidence for segregation of timing and velocity storage in predictive oculomotor control

    Exp. Brain Res.

    (1999)
  • G.R. Barnes et al.

    Sequence learning in human ocular smooth pursuit

    Exp. Brain Res.

    (2002)
  • G.R. Barnes et al.

    Volitional control of anticipatory ocular smooth pursuit after viewing, but not pursuing, a moving target: evidence for a re-afferent velocity store

    Exp. Brain Res.

    (1997)
  • G.R. Barnes et al.

    Ocular pursuit responses to repeated, single-cycle sinusoids reveal behavior compatible with predictive pursuit

    J. Neurophysiol.

    (2000)
  • S.J. Bennett et al.

    Human ocular pursuit during the transient disappearance of a visual target

    J. Neurophysiol.

    (2003)
  • C. Buchel et al.

    The functional anatomy of attention to visual motion: a functional MRI study

    Brain

    (1998)
  • J. Carl et al.

    Human smooth pursuit: stimulus-dependent responses

    J. Neurophysiol.

    (1987)
  • K.J. Cole et al.

    Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp

    Exp. Brain Res.

    (2002)
  • C.J.S. Collins et al.

    Scaling of anticipatory smooth eye velocity in response to sequences of discrete target movements in humans

    Abstr. - Soc. Neurosci.

    (2003)
  • M.H.E. de Lussanet et al.

    The effect of expectations on hitting moving targets: influence of the preceding target's speed

    Exp. Brain Res.

    (2001)
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