ERP evidence for selective drop in attentional costs in uncertain environments: challenging a purely premotor account of covert orienting of attention

Several studies have proved that the reliability of endogenous spatial cues linearly modulates the reaction time advantage in the processing of targets at validly cued vs. invalidly cued locations, i.e. the "validity effect". This would imply that with non-predictive cues, no "validity effect" should be observed. However, contrary to this prediction, one could hypothesize that attentional benefits by valid cuing (i.e. the RT advantage for validly vs. neutrally cued targets) can still be maintained with non-predictive cues, if the brain were endowed with mechanisms allowing the selective reduction in costs of reorienting from invalidly cued locations (i.e. the reduction of the RT disadvantage for invalidly vs. neutrally cued targets). This separated modulation of attentional benefits and costs would be adaptive in uncertain contexts where cues predict at chance level the location of targets. Through the joint recording of manual reaction times and event-related cerebral potentials (ERPs), we have found that this is the case and that relying on non-predictive endogenous cues results in abatement of attentional costs and the difference in the amplitude of the P1 brain responses evoked by invalidly vs. neutrally cued targets. In contrast, the use of non-predictive cues leaves unaffected attentional benefits and the difference in the amplitude of the N1 responses evoked by validly vs. neutrally cued targets. At the individual level, the drop in costs with non-predictive cues was matched with equivalent lateral biases in RTs to neutrally and invalidly cued targets presented in the left and right visual field. During the cue period, the drop in costs with non-predictive cues was preceded by reduction of the Early Directing Attention Negativity (EDAN) on posterior occipital sites and by enhancement of the frontal Anterior Directing Attention Negativity (ADAN) correlated to preparatory voluntary orienting. These findings demonstrate, for the first time, that the segregation of mechanisms regulating attentional benefits and costs helps efficiency of orienting in "uncertain" visual spatial contexts characterized by poor probabilistic association between cues and targets.