Unconscious Neural Activity Predicts Overt Attention in Visual Search

Abstract Unconscious neural activity has been shown to precede both motor and cognitive acts. In the present study, we investigated the neural antecedents of overt attention during visual search, where subjects make voluntary saccadic eye movements to search a cluttered stimulus array for a target item. Building on studies of both overt self-generated motor actions (Lau et al., 2004, Soon et al., 2008) and self-generated cognitive actions (Bengson et al., 2014, Soon et al., 2013), we hypothesized that brain activity prior to the onset of a search array would predict the direction of the first saccade during unguided visual search. Because both spatial attention and gaze are coordinated during visual search, both cognition and motor actions are coupled during visual search. A well-established finding in fMRI studies of willed action is that neural antecedents of the intention to make a motor act (e.g., reaching) can be identified seconds before the action occurs. Studies of the volitional control of covert spatial attention in EEG have shown that predictive brain activity is limited to only a few hundred milliseconds before a voluntary shift of covert spatial attention. In the present study, the visual search task and stimuli were designed so that subjects could not predict the onset of the search array. Perceptual task difficulty was high, such that they could not locate the target using covert attention alone, thus requiring overt shifts of attention (saccades) to carry out the visual search. If the first saccade to the array onset in unguided visual search shares mechanisms with willed shifts of covert attention, we expected predictive EEG alpha-band activity (8-12 Hz) immediately prior to the array onset (within 1 sec) (Bengson et al., 2014; Nadra et al., 2023). Alternatively, if they follow the principles of willed motor actions, predictive neural signals should be reflected in broadband EEG activity (Libet et al., 1983) and would likely emerge earlier (Soon et al., 2008). Applying support vector machine decoding, we found that the direction of the first saccade in an unguided visual search could be predicted up to two seconds preceding the search array’s onset in the broadband but not alpha-band EEG. These findings suggest that self-directed eye movements in visual search emerge from early preparatory neural activity more akin to willed motor actions than to covert willed attention. This highlights a distinct role for unconscious neural dynamics in shaping visual search behavior.