The orbitofrontal-anterior temporal network complements the attention network for where to look in social situations.

Abstract

Human neuroimaging experiments have consistently found dorsal and ventral attention networks subserving spatial shifts of covert attention or eye movements. However, these experiments used abstract, artificial stimuli for better experimental stimulus control and clearly defined instructions about where to attend or what to search for. This clearly is not an adequate model of eye movement control in natural environments full of semantic and social information. Here, we show that during movie viewing, activation of the dorsal and ventral attention networks was complemented by activation patterns in orbitofrontal and anterior temporal cortex, previously not implicated in human eye movement control, supporting individual decisions where to look. This effect was largely driven by looking at faces. We compared similarity relationships between eye fixation patterns on the one hand and brain activity patterns on the other hand in human participants of either sex. Searching for between-scenes changes in activation patterns that mirrored changes in fixation patterns, we were able to identify the attention networks defined by previous experiments with artificial stimuli. In contrast, interindividual differences in fixation patterns, indicative of endogenous decisions about where to look, were mirrored by activation pattern differences in orbitofrontal and anterior temporal cortex, particularly for scenes presenting faces. Thus, we could precisely replicate the role of the attention networks in a more natural viewing environment. Crucially, we also showed that previous lab experiments, lacking the complexity of free viewing in a naturalistic environment, overlooked the importance of the orbitofrontal - anterior temporal network for individual differences in active vision. Our findings show that the orbitofrontal - anterior temporal network needs to be considered in studies of active vision, particularly in social situations.Significance Statement Human attention networks have been replicated in a naturalistic setting. The attention networks could be mapped by comparing the similarity of fixation patterns and local brain activation patterns between scenes of a movie. In contrast, searching for brain activation reflecting interindividual differences in fixation patterns yielded an orbitofrontal-anterior temporal network. This network showed the highest similarity of fixation and brain activation patterns during scens containing faces, in line with its known function for social communication.