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The Journal of Neuroscience, August 26, 2009, 29(34):10683-10694; doi:10.1523/JNEUROSCI.0673-09.2009

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Behavioral/Systems/Cognitive
Modulation of the Contrast Response Function by Electrical Microstimulation of the Macaque Frontal Eye Field

Leeland B. Ekstrom,^1,3,4 Pieter R. Roelfsema,^5,6 John T. Arsenault,^1,7 Hauke Kolster,^1,7 and Wim Vanduffel^1,2,7

¹Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, and ²Department of Radiology, Harvard Medical School, Charlestown, Massachusetts 02129, ³Harvard-Massachusetts Institute of Technology Division of Health Sciences and Technology and ⁴Department of Nuclear Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, ⁵Department of Vision and Cognition, The Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, The Netherlands, ⁶Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081 HV Amsterdam, The Netherlands, and ⁷Laboratorium voor Neuro- en Psychofysiologie, Medical School, Campus Gasthuisberg, Katholieke Universiteit Leuven, 3000 Leuven, Belgium

Correspondence should be addressed to Dr. Wim Vanduffel, Athinoula A. Martinos Center for Biomedical Imaging, 149 13th Street, Suite 2300, Charlestown, MA 02129. Email: wim{at}nmr.mgh.harvard.edu

Spatial attention influences representations in visual cortical areas as well as perception. Some models predict a contrast gain, whereas others a response or activity gain when attention is directed to a contrast-varying stimulus. Recent evidence has indicated that microstimulating the frontal eye field (FEF) can produce modulations of cortical area V4 neuronal firing rates that resemble spatial attention-like effects, and we have shown similar modulations of functional magnetic resonance imaging (fMRI) activity throughout the visual system. Here, we used fMRI in awake, fixating monkeys to first measure the response in 12 visual cortical areas to stimuli of varying luminance contrast. Next, we simultaneously microstimulated subregions of the FEF with movement fields that overlapped the stimulus locations and measured how microstimulation modulated these contrast response functions (CRFs) throughout visual cortex. In general, we found evidence for a nonproportional scaling of the CRF under these conditions, resembling a contrast gain effect. Representations of low-contrast stimuli were enhanced by stimulation of the FEF below the threshold needed to evoke saccades, whereas high-contrast stimuli were unaffected or in some areas even suppressed. Furthermore, we measured a characteristic spatial pattern of enhancement and suppression across the cortical surface, from which we propose a simple schematic of this contrast-dependent fMRI response.

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Received Feb. 5, 2009; revised July 5, 2009; accepted July 15, 2009.

Correspondence should be addressed to Dr. Wim Vanduffel, Athinoula A. Martinos Center for Biomedical Imaging, 149 13th Street, Suite 2300, Charlestown, MA 02129. Email: wim{at}nmr.mgh.harvard.edu

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