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Beta and theta oscillations differentially support free versus forced control over multiple-target search

View ORCID ProfileJoram van Driel, View ORCID ProfileEduard Ort, Johannes J. Fahrenfort, View ORCID ProfileChristian N. L. Olivers
doi: https://doi.org/10.1101/422691
Joram van Driel
1Department of Experimental and Applied Psychology, Institute for Brain and Behavior, Vrije Universiteit Amsterdam, The Netherlands
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Eduard Ort
1Department of Experimental and Applied Psychology, Institute for Brain and Behavior, Vrije Universiteit Amsterdam, The Netherlands
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Johannes J. Fahrenfort
1Department of Experimental and Applied Psychology, Institute for Brain and Behavior, Vrije Universiteit Amsterdam, The Netherlands
2Department of Psychology, Amsterdam Brain and Cognition, University of Amsterdam, The Netherlands
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Christian N. L. Olivers
1Department of Experimental and Applied Psychology, Institute for Brain and Behavior, Vrije Universiteit Amsterdam, The Netherlands
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Abstract

Many important situations require human observers to simultaneously search for more than one object. Despite a long history of research into visual search, the behavioral and neural mechanisms associated with multiple-target search are poorly understood. Here we test the novel theory that the efficiency of looking for multiple targets critically depends on the mode of cognitive control the environment affords to the observer. We used an innovative combination of EEG and eye tracking while participants searched for two targets, within two different contexts: Either both targets were present in the search display and observers were free to prioritize either one of them, thus enabling proactive control over selection; or only one of the two targets would be present in each search display, which requires reactive control to reconfigure selection when the wrong target is prioritized. During proactive control, both univariate and multivariate signals of beta-band (15–35 Hz) power suppression prior to display onset predicted switches between target selections. This signal originated over midfrontal and sensorimotor regions and has previously been associated with endogenous state changes. In contrast, imposed target selections requiring reactive control elicited prefrontal power enhancements in the delta/theta-band (2–8 Hz), but only after display onset. This signal predicted individual differences in associated oculomotor switch costs, reflecting reactive reconfiguration of target selection. The results provide compelling evidence that multiple target representations are differentially prioritized during visual search, and for the first time reveal distinct neural mechanisms underlying proactive and reactive control over multiple-target search.

Significance Statement Searching for more than one object in complex visual scenes can be detrimental for search performance. While perhaps annoying in daily life, this can have severe consequences in professional settings such as medical and security screening. Previous research has not yet resolved whether multiple-target search involves changing priorities in what people attend to, and how such changes are controlled. We approached these questions by concurrently measuring cortical activity and eye movements using EEG and eye tracking, while observers searched for multiple possible targets. Our findings provide the first unequivocal support for the existence of two modes of control during multiple-target search, which are expressed in qualitatively distinct time-frequency signatures of the EEG both before and after visual selection.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted September 24, 2018.
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Beta and theta oscillations differentially support free versus forced control over multiple-target search
Joram van Driel, Eduard Ort, Johannes J. Fahrenfort, Christian N. L. Olivers
bioRxiv 422691; doi: https://doi.org/10.1101/422691
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Beta and theta oscillations differentially support free versus forced control over multiple-target search
Joram van Driel, Eduard Ort, Johannes J. Fahrenfort, Christian N. L. Olivers
bioRxiv 422691; doi: https://doi.org/10.1101/422691

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