Beta and Theta Oscillations Differentially Support Free Versus Forced Control over Multiple-Target Search.

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 electroencephalogram (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 has been prioritized. During proactive control, both univariate and multivariate signals of beta-band (15-35 Hz) power suppression before 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. Although 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.