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Transcranial magnetic stimulation of macaque frontal eye fields decreases saccadic reaction time

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A Correspondence to this article was published on 07 September 2011

Abstract

Transcranial magnetic stimulation (TMS) is increasingly used to perturb targeted human brain sites non-invasively, to test for causal effects on performance of cognitive tasks. TMS might also be used in non-human primates to complement invasive work and compare with human studies. Here, we targeted the frontal eye fields (FEF) in two macaques with a continuous theta-burst (cTBS) protocol, testing the impact on visually guided saccades. After unilateral cTBS over the FEF in either hemisphere, a small (mean 7 ms) but highly consistent decrease in saccadic reaction times (RTs) was observed. Lower latencies arose for saccades both contra- and ipsilateral to the stimulated FEF after cTBS. These results provide the first demonstration that TMS can be used to affect saccadic behavior in non-human primates. The unexpectedly bilateral impact on RTs may reflect an impact on ‘fixation’ neurons in the FEF and/or transcallosal modulation of both FEFs induced by unilateral cTBS. In either case, this study demonstrates a clear behavioral effect induced by TMS in awake behaving monkeys performing a cognitive task. This opens new opportunities for investigating the causal roles of targeted brain areas in behavior, for measuring physiological consequences of TMS in the primate brain, and ultimately for human–monkey comparisons.

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Acknowledgments

The authors are indebted to A. Coeman, C. Fransen, M. Depaep, W. Depuydt, M. Deforche, P. Kayenbergh, G. Meulemans, C. Van Eupen, S. Verstraeten for help with the experiments. The work was supported by Human Frontiers Science Program (HFSPO RGP7/2007), Medical Foundation Queen Elisabeth (2008-10), Inter University Attraction Pole6/29, Program Financing 2010-15, Fonds voor Wetenschappelijk onderzoek, VLaanderen (FWO) G.0622.08; FWO G.0593.09, National Science Foundation BCS-0745436 and European Union (EU) grant (FP7 HEALTH-F2-2008-200728), BrainSynch. JD is a Royal Society Anniversary Research Professor. AG has an Aspirant fellowship of FWO-Flanders.

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Authors and Affiliations

  1. Laboratory for Neuro-and Psychophysiology, K.U. Leuven Medical School, Campus Gasthuisberg, Leuven, Belgium

    Annelies Gerits, Olivier Guipponi & Wim Vanduffel

  2. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, 02129, USA

    Annelies Gerits & Wim Vanduffel

  3. Department of Radiology, Harvard Medical School, Charlestown, MA, USA

    Annelies Gerits & Wim Vanduffel

  4. Laboratory for Movement Control and Neuroplasticity, K.U. Leuven, Leuven, Belgium

    Nicole Wenderoth

  5. Laboratory for Social and Neural Systems Research (SNS-lab), Zurich, Switzerland

    Christian C. Ruff

  6. UCL Institute of Cognitive Neuroscience, London, UK

    Christian C. Ruff & Jon Driver

  7. Wellcome Trust Centre for Neuroimaging at UCL, London, UK

    Christian C. Ruff & Jon Driver

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  1. Annelies Gerits
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  2. Christian C. Ruff
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  3. Olivier Guipponi
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  4. Nicole Wenderoth
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  5. Jon Driver
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  6. Wim Vanduffel
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Correspondence to Wim Vanduffel.

Additional information

A. Gerits and C. C. Ruff these authors contributed equally.

A comment to this article is available at http://dx.doi.org/10.1007/s00221-011-2840-7.

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221_2011_2710_MOESM2_ESM.eps

Fig. S1 Schematic drawing of a monkey-TMS setup based on a picture. The left panel of the figure shows the D25mm TMS coil with its center positioned above the monkey’s right FEF. The position was determined using the brainsight neuronavigation system. The head of the monkey was fixed to the chair. In the right panel the size of TMS coil in respect to the monkey’s head size can be observed. (EPS 10892 kb)

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Gerits, A., Ruff, C.C., Guipponi, O. et al. Transcranial magnetic stimulation of macaque frontal eye fields decreases saccadic reaction time. Exp Brain Res 212, 143–152 (2011). https://doi.org/10.1007/s00221-011-2710-3

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  • DOI: https://doi.org/10.1007/s00221-011-2710-3

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