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Neck muscle responses evoked by transcranial magnetic stimulation of the human frontal eye fields

Authors

  • Samanthi C. Goonetilleke,

    1. Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada N6A 5C1
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  • Paul L. Gribble,

    1. Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada N6A 5C1
    2. Department of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C1
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  • Seyed M. Mirsattari,

    1. Department of Clinical Neurological Sciences, University of Western Ontario, London, Ontario, Canada N6A 5C1
    2. Department of Medical Biophysics, University of Western Ontario, London, Ontario, Canada N6A 5C1
    3. Department of Medical Imaging, University of Western Ontario, London, Ontario, Canada N6A 5C1
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  • Timothy J. Doherty,

    1. Department of Clinical Neurological Sciences, University of Western Ontario, London, Ontario, Canada N6A 5C1
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  • Brian D. Corneil

    1. Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada N6A 5C1
    2. Department of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C1
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    • Present address: Centre for Brain and Mind, Robarts Research Institute, London, Ontario, Canada N6A 5K8.


Brian D. Corneil, *present address below.
E-mail: bcorneil@uwo.ca

Abstract

Transcranial magnetic stimulation (TMS) provides a non-invasive means of investigating brain function. Whereas TMS of the human frontal eye fields (FEFs) does not induce saccades, electrical stimulation of the monkey FEF evokes eye–head gaze shifts, with neck muscle responses evoked at stimulation levels insufficient to evoke a saccade. These animal results motivated us to examine whether TMS of the FEF (TMS-FEF) in humans evokes a neck muscle response. Subjects performed memory-guided saccades to the left or right while TMS (two pulses at 20 Hz) was delivered on 30% of trials to the left FEF coincident with saccade instruction. As reported previously, TMS-FEF decreased contralateral saccade reaction times. We simultaneously recorded the activity of splenius capitis (SPL) (an ipsilateral head turner). TMS-FEF evoked a lateralized increase in the activity of the right SPL but not the left SPL, consistent with the recruitment of a contralateral head-turning synergy. In some subjects, the evoked neck muscle response was time-locked to stimulation, whereas in others the evoked response occurred around the time of the saccade. Importantly, evoked responses were greater when TMS was applied to the FEF engaged in contralateral saccade preparation, with even greater evoked responses preceding shorter latency saccades. These results provide new insights into both the nature of TMS and the human oculomotor system, demonstrating that TMS-FEF engages brainstem oculomotor circuits in a manner consistent with a general role in eye–head gaze orienting. Our results also suggest that pairing neck muscle recordings with TMS-FEF provides a novel way of assaying the covert preparation of oculomotor plans.

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