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PLoS Biol. 2016 Mar 25;14(3):e1002420. doi: 10.1371/journal.pbio.1002420. eCollection 2016 Mar.

The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex.

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Department of Vision and Cognition, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Art and Sciences (KNAW), Amsterdam, the Netherlands.
Cognitive Neuroscience Department, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, the Netherlands.
Department of Neuroimaging and Neuromodeling, Netherlands Institute for Neuroscience, an institute of the Royal Netherlands Academy of Art and Sciences (KNAW), Amsterdam, the Netherlands.
Department of Clinical Neurophysiology, VU University Medical Center, Amsterdam, the Netherlands.
Université de Toulouse, Centre de Recherche Cerveau et Cognition, Université Paul Sabatier, Toulouse, France.
CNRS, UMR 5549, Faculté de Médecine de Purpan, Toulouse, France.
Department of Clinical Neurophysiology, Stichting Epilepsie Instelling Nederland, Heemstede, the Netherlands.
Department of Neurosurgery, VU University Medical Center, Amsterdam, the Netherlands.
Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, VU University, Amsterdam, The Netherlands.
Psychiatry department, Academic Medical Center, Amsterdam, The Netherlands.


Here we report the first quantitative analysis of spiking activity in human early visual cortex. We recorded multi-unit activity from two electrodes in area V2/V3 of a human patient implanted with depth electrodes as part of her treatment for epilepsy. We observed well-localized multi-unit receptive fields with tunings for contrast, orientation, spatial frequency, and size, similar to those reported in the macaque. We also observed pronounced gamma oscillations in the local-field potential that could be used to estimate the underlying spiking response properties. Spiking responses were modulated by visual context and attention. We observed orientation-tuned surround suppression: responses were suppressed by image regions with a uniform orientation and enhanced by orientation contrast. Additionally, responses were enhanced on regions that perceptually segregated from the background, indicating that neurons in the human visual cortex are sensitive to figure-ground structure. Spiking responses were also modulated by object-based attention. When the patient mentally traced a curve through the neurons' receptive fields, the accompanying shift of attention enhanced neuronal activity. These results demonstrate that the tuning properties of cells in the human early visual cortex are similar to those in the macaque and that responses can be modulated by both contextual factors and behavioral relevance. Our results, therefore, imply that the macaque visual system is an excellent model for the human visual cortex.

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