Journal Article

Disparate substrates for head gaze following and face perception in the monkey superior temporal sulcus

Atabaki, Artin, Thier, Peter, Marciniak, Karolina, Dicke, Peter W

2014

Overview

Primates use gaze cues to follow peer gaze to an object of joint attention. Gaze following of monkeys is largely determined by head or face orientation. We used fMRI in rhesus monkeys to identify brain regions underlying head gaze following and to assess their relationship to the ‘face patch’ system, the latter being the likely source of information on face orientation. We trained monkeys to locate targets by either following head gaze or using a learned association of face identity with the same targets. Head gaze following activated a distinct region in the posterior STS, close to-albeit not overlapping with-the medial face patch delineated by passive viewing of faces. This ‘gaze following patch’ may be the substrate of the geometrical calculations needed to translate information on head orientation from the face patches into precise shifts of attention, taking the spatial relationship of the two interacting agents into account. Gaze following—working out where someone else is looking, and then switching your attention to that position—is an important part of social behavior and learning. Additionally, it is thought to be an important step towards recognizing that others have a mind of their own. Humans mostly use eye position to work out the ‘gaze direction’ of someone else, whereas non-human primates rely instead on the orientation of the face. However, the neural circuits that control gaze following are thought to be similar in both. Gaze following is a complex process that requires the brain to process a lot of different information. A face must be recognized, and its orientation worked out. A series of complex geometrical calculations must then be performed to work out the direction of the gaze, and how this relates to the position of the observer. Finally, the object of interest needs to be recognized and the attention of the observer focused on it. In the monkey brain, there are six interconnected areas called face patch regions that respond when a monkey is shown a face. However, researchers do not understand how monkeys translate the information about face orientation gathered by these regions into information about where to look during gaze following. Marciniak et al. performed functional magnetic resonance imaging on monkeys to track the flow of blood to different regions of the brain—the higher the blood flow, the more that area of the brain is working. To identify the location of their face patch regions, the monkeys first looked at faces. When the monkeys then performed a gaze following task, a region of the brain close to—but not overlapping—the face patches was activated. Marciniak et al. suggest this is the ‘gaze following patch’ where the brain performs the demanding calculations to translate face orientation into a position to look at. As gaze following is important in social interactions, understanding the neural circuits behind it could help us understand social disorders.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Attention / Behavior, Animal / Brain mapping / Computer Simulation / Cues / Experiments / Face / face patches / Fixation, Ocular / Functional magnetic resonance imaging / gaze following / Head / joint attention / Macaca mulatta / macaque monkey / Magnetic Resonance Imaging / monkey fMRI / Monkeys & apes / Neuroscience / Orientation / Pattern recognition / Pattern Recognition, Automated / Photic Stimulation / social attention / Superior temporal sulcus / Temporal Lobe - anatomy & histology / Temporal Lobe - physiology / Vision, Ocular / Visual Perception