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Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control

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Abstract

This study examined the extent to which human subjects predict future target motion for the control of smooth ocular pursuit. Subjects were required to pursue an accelerating target (0, 4 or 8°/s2) that underwent a transient occlusion, and consequently reappeared with the same or increased velocity. Presentations were received in a random or blocked order. Subjects exhibited anticipatory smooth pursuit prior to target motion onset, which in blocked presentations was scaled to the velocity generated by the target acceleration. In random presentations subjects also exhibited anticipatory smooth pursuit, but this was reflected in a more generalized response. During the transient occlusion all subjects exhibited a reduction in eye velocity, which was followed in the majority by a recovery prior to target reappearance. In random presentations, eye velocity decayed and recovered to a level that followed on from the response to the initial ramp. In blocked presentations, there was evidence of improved scaling throughout, which culminated in a significant increase in eye velocity between the start and end of the transient occlusion (8°/s2 only). These findings are difficult to reconcile with reflexive accounts of oculomotor control that perpetuate current eye motion, and hence generate a simple form of prediction using a direct efference copy (“eye-velocity memory”). Rather, they are more consistent with the scaling of smooth pursuit eye movements by means of a more-persistent velocity-based representation, which plays a significant role in both random and blocked stimulus presentations.

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Notes

  1. The term “reflexive” control as used here refers to ocular pursuit movements that are initially driven by visual feedback and then perpetuated by the direct efference copy loop (Krauzlis and Lisberger 1994; Leigh and Zee 1991). We suggest that “voluntary” control represents a continuum from low-level to high-level control and is an adaptive process that enables an individual to generate a tuned response, often in the absence of sensory input (e.g., anticipatory smooth pursuit).

  2. The term “velocity-based” is used because the direct and indirect loops receive input from retinal velocity error (i.e., retinal slip) when the participant pursues a moving target, or holds fixation in the presence of a moving target. In both cases, the velocity-based information accumulated does not equate to an allocentric representation of target velocity, but rather it represents an estimate of target image velocity.

  3. A potential drawback of the arrangement proposed by Bennett and Barnes (2004) was that the setting of the variable gain function was influenced by both the loss of visual feedback (Conflict Detector) as well as expectation regarding the step change in target velocity. This makes it difficult to independently modulate the response, such as is necessary in sequence learning experiments, where target velocity is scaled to each ramp within the sequence but there is no loss of visual feedback (pursuing a sinusoidal trajectory presents a similar situation).

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Acknowledgements

This work was funded by the Medical Research Council, UK

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Authors and Affiliations

  1. Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, The Henry Cotton Building, 15-21 Webster Street, Liverpool, L3 2ET, UK

    Simon J. Bennett

  2. Faculty of Life Sciences, University of Manchester, Moffat Building, Sackville St., Manchester, M60 1QD, UK

    Simon J. Bennett & Graham R. Barnes

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  1. Simon J. Bennett
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  2. Graham R. Barnes
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Correspondence to Simon J. Bennett.

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Bennett, S.J., Barnes, G.R. Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control. Exp Brain Res 175, 1–10 (2006). https://doi.org/10.1007/s00221-006-0533-4

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  • DOI: https://doi.org/10.1007/s00221-006-0533-4

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