Frontal eye fields control attentional modulation of alpha and gamma oscillations in contralateral occipitoparietal cortex

Research output: Contribution to journalArticle

Authors

  • Tom R Marshall
  • Ole Jensen
  • Jacinta O'Shea
  • Til O Bergmann

External organisations

  • Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, t.marshall@donders.ru.nl.
  • Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, United Kingdom, and.
  • Donders Institute for Brain, Cognition, and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, Institute of Psychology, Christian-Albrechts University of Kiel, 24118 Kiel, Germany.

Abstract

Covertly directing visuospatial attention produces a frequency-specific modulation of neuronal oscillations in occipital and parietal cortices: anticipatory alpha (8-12 Hz) power decreases contralateral and increases ipsilateral to attention, whereas stimulus-induced gamma (>40 Hz) power is boosted contralaterally and attenuated ipsilaterally. These modulations must be under top-down control; however, the control mechanisms are not yet fully understood. Here we investigated the causal contribution of the human frontal eye field (FEF) by combining repetitive transcranial magnetic stimulation (TMS) with subsequent magnetoencephalography. Following inhibitory theta burst stimulation to the left FEF, right FEF, or vertex, participants performed a visual discrimination task requiring covert attention to either visual hemifield. Both left and right FEF TMS caused marked attenuation of alpha modulation in the occipitoparietal cortex. Notably, alpha modulation was consistently reduced in the hemisphere contralateral to stimulation, leaving the ipsilateral hemisphere relatively unaffected. Additionally, right FEF TMS enhanced gamma modulation in left visual cortex. Behaviorally, TMS caused a relative slowing of response times to targets contralateral to stimulation during the early task period. Our results suggest that left and right FEF are causally involved in the attentional top-down control of anticipatory alpha power in the contralateral visual system, whereas a right-hemispheric dominance seems to exist for control of stimulus-induced gamma power. These findings contrast the assumption of primarily intrahemispheric connectivity between FEF and parietal cortex, emphasizing the relevance of interhemispheric interactions. The contralaterality of effects may result from a transient functional reorganization of the dorsal attention network after inhibition of either FEF.

Details

Original languageEnglish
Pages (from-to)1638-1647
Number of pages10
JournalThe Journal of Neuroscience
Volume35
Issue number4
Publication statusPublished - 28 Jan 2015

Keywords

  • Dorsal attentional network, Frontal eye field, Magnetoencephalography, Transcranial magnetic stimulation, Visual attention