Search for a threatening target triggers limbic guidance of spatial attention

The ability to actively locate potential threats in our environment is highly adaptive. To investigate mediating neural mechanisms, we designed a visual search task in which central cues signaled future location and emotional expression (angry or neutral) of a target face. Cues predicting angry targets accelerated subsequent attention shifts, indicating that endogenous signals predicting threatening events can prime the spatial attention network. Functional imaging showed that spatially informative cues activated the fusiform gyrus (FG) as well as frontoparietal components of the spatial attention network, including intraparietal sulcus (IPS) and frontal eye field (FEF), whereas cues predicting angry faces also activated limbic areas, including the amygdala. Anatomically overlapping, additive effects of spatial and emotional cuing were identified in the IPS, FEFs, and FG, regions that also displayed augmented connectivity with the amygdala after cues predicting angry faces. These data highlight a key role for the frontoparietal spatial attention network in the compilation of a salience map that combines the spatial coordinates of an event with its motivational relevance. Furthermore, they suggest that active search for a threatening stimulus elicits amygdala input to the spatial attention network and inferotemporal visual areas, facilitating the rapid detection of upcoming motivationally significant events.