Expectancies Influence Attention to Neutral But Not Necessarily to Threatening Stimuli: An fMRI Study

Recent behavioral observations suggest an influence of prior expectancies on attention to neutral targets, whereas the detection of threatening targets remains comparably immune to these expectancies. The origin of this asymmetry, however, remains unclear. Here, therefore, we investigated its neural basis by using fMRI. Specifically, we tested whether, in accordance with the idea of a resetting attentional system during phylogenetic threat detection, neural responses for threatening compared with neutral targets would remain largely unaffected by prior expectancies. Alternatively, neural responses could reflect equally strong expectancy influences on both types of targets, with the respective patterns differing, thereby producing the asymmetric effect observed in behavior. Predictive cues in our study evoked specific behavioral and neural expectancy states and effectively modulated response latencies to detect neutral (bird) targets in a 3 x 3 visual search matrix: When threat-related (spider) rather than neutral targets were expected, bird detection was considerably slowed, and the neural response to expected birds differed from that to unexpected birds. Conversely, and in line with the hypothesis of a resetting attentional system for phylogenetic threat, expectancy cues had no impact on RTs or neural responses for spider targets-either in spider phobic participants or in non-spider-fearful control participants. Our data support the idea of bottom-up enhancement of threat-related information through processing pathways unaffected by top-down modulatory influences such as expectancy. These pathways may subserve rapid and comparably automatic responding to threat stimuli by safeguarding independence from more controlled and explicit expectancies, consequently promoting adaptive behavior and survival.