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An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans

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Abstract

Both optokinetic nystagmus (OKN) and smooth-pursuit eye movements (SPEM) are subclasses of so-called slow eye movements. However, optokinetic responses are reflexive whereas smooth pursuit requires the voluntary tracking of a moving target. We used functional magnetic resonance imaging (fMRI) to determine the neural basis of OKN and SPEM, and to uncover whether the two underlying neural systems overlap or are independent at the cortical level. The results showed a largely overlapping neural circuitry. A direct comparison between activity during the execution of OKN and SPEM yielded no oculomotor-related area exclusively dedicated to one or the other eye movement type. Furthermore, the performance of SPEM evoked a bilateral deactivation of the human equivalent of the parietoinsular vestibular cortex. This finding might indicate that the reciprocally inhibitory visual–vestibular interaction involves not only OKN but also SPEM, which are both linked with the encoding of object-motion and self-motion. Moreover, we could show differential activation patterns elicited by look-nystagmus and stare-nystagmus. Look-nystagmus is characterized by large amplitudes and low-frequency resetting eye movements rather resembling SPEM. Look-nystagmus evoked activity in cortical oculomotor centers. By contrast, stare-nystagmus is usually characterized as being more reflexive in nature and as showing smaller amplitudes and higher frequency resetting eye movements. Stare-nystagmus failed to elicit significant signal changes in the same regions as look-nystagmus/SPEM. Thus, less reflexive eye movements correlated with more pronounced signal intensity. Finally, on the basis of a general investigation of slow eye movements, we were interested in a cortical differentiation between subtypes of SPEM. We compared activity associated with predictable and unpredictable SPEM as indicated by appropriate visual cues. In general, predictable and unpredictable SPEM share the same neural network, yet information about the direction of an upcoming target movement reduced the cerebral activity level.

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Abbreviations

BA:

Brodmann area

fMRI:

Functional magnetic resonance imaging

FEF:

Frontal eye field

GLM:

General linear model

MP-RAGE:

Magnetization-prepared rapid acquisition gradient echo

OKN:

Optokinetic nystagmus

pIP:

Posterior intraparietal area

PIVC:

Parietoinsular vestibular cortex

pSPL:

Posterior portion of the superior parietal lobule

SEF:

Supplementary eye field

SPEM:

Smooth-pursuit eye movement

VIP:

Ventral intraparietal area

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Acknowledgements

This research was supported by HFSP (RG0149/1999-B), EU-Eurokinesis (QLRT-2001-00151), and SFB 194 (A 13). The authors thank Erika Raedisch for excellent technical assistance.

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Authors and Affiliations

  1. Department of Neurophysics, Philipps-University Marburg, Renthof 7, 35032, Marburg, Germany

    Christina S. Konen & Frank Bremmer

  2. Department of Neurology, Heinrich-Heine-University Düsseldorf, Germany

    Raimund Kleiser & Rüdiger J. Seitz

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  1. Christina S. Konen
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  2. Raimund Kleiser
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  4. Frank Bremmer
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Correspondence to Christina S. Konen.

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Konen, C.S., Kleiser, R., Seitz, R.J. et al. An fMRI study of optokinetic nystagmus and smooth-pursuit eye movements in humans. Exp Brain Res 165, 203–216 (2005). https://doi.org/10.1007/s00221-005-2289-7

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