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The Journal of Neuroscience, April 30, 2008, 28(18):4823-4835; doi:10.1523/JNEUROSCI.4499-07.2008

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Behavioral/Systems/Cognitive
The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4

Pascal Fries,^1,2 * Thilo Womelsdorf,^1 * Robert Oostenveld,¹ and Robert Desimone^3,4

¹F. C. Donders Centre for Cognitive Neuroimaging, Radboud University Nijmegen, 6525 EN Nijmegen, The Netherlands, ²Department of Biophysics, Radboud University Nijmegen, 6525 EZ Nijmegen, The Netherlands, ³Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, and ⁴McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Correspondence should be addressed to Dr. Pascal Fries, F. C. Donders Centre for Cognitive Neuroimaging, Kapittelweg 29, 6525 EN Nijmegen, The Netherlands. Email: pascal.fries{at}fcdonders.ru.nl

Selective attention lends relevant sensory input priority access to higher-level brain areas and ultimately to behavior. Recent studies have suggested that those neurons in visual areas that are activated by an attended stimulus engage in enhanced gamma-band (30–70 Hz) synchronization compared with neurons activated by a distracter. Such precise synchronization could enhance the postsynaptic impact of cells carrying behaviorally relevant information. Previous studies have used the local field potential (LFP) power spectrum or spike-LFP coherence (SFC) to indirectly estimate spike synchronization. Here, we directly demonstrate zero-phase gamma-band coherence among spike trains of V4 neurons. This synchronization was particularly evident during visual stimulation and enhanced by selective attention, thus confirming the pattern inferred from LFP power and SFC. We therefore investigated the time course of LFP gamma-band power and found rapid dynamics consistent with interactions of top-down spatial and feature attention with bottom-up saliency. In addition to the modulation of synchronization during visual stimulation, selective attention significantly changed the prestimulus pattern of synchronization. Attention inside the receptive field of the recorded neuronal population enhanced gamma-band synchronization and strongly reduced -band (9–11 Hz) synchronization in the prestimulus period. These results lend further support for a functional role of rhythmic neuronal synchronization in attentional stimulus selection.

Key words: synchronization; oscillation; coherence; gamma; ; attention

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Received Oct. 2, 2007; revised Feb. 12, 2008; accepted March 30, 2008.

Correspondence should be addressed to Dr. Pascal Fries, F. C. Donders Centre for Cognitive Neuroimaging, Kapittelweg 29, 6525 EN Nijmegen, The Netherlands. Email: pascal.fries{at}fcdonders.ru.nl

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