Abstract
Quantifying attention to social stimuli during the viewing of complex social scenes with eye tracking has proven to be a sensitive method in the diagnosis of autism spectrum disorders years before average clinical diagnosis. Rhesus macaques provide an ideal model for understanding the mechanisms underlying social viewing behavior, but to date no comparable behavioral task has been developed for use in monkeys. Using a novel scene-viewing task, we monitored the gaze of three rhesus macaques while they freely viewed well-controlled composed social scenes and analyzed the time spent viewing objects and monkeys. In each of six behavioral sessions, monkeys viewed a set of 90 images (540 unique scenes) with each image presented twice. In two-thirds of the repeated scenes, either a monkey or an object was replaced with a novel item (manipulated scenes). When viewing a repeated scene, monkeys made longer fixations and shorter saccades, shifting from a rapid orienting to global scene contents to a more local analysis of fewer items. In addition to this repetition effect, in manipulated scenes, monkeys demonstrated robust memory by spending more time viewing the replaced items. By analyzing attention to specific scene content, we found that monkeys strongly preferred to view conspecifics and that this was not related to their salience in terms of low-level image features. A model-free analysis of viewing statistics found that monkeys that were viewed earlier and longer had direct gaze and redder sex skin around their face and rump, two important visual social cues. These data provide a quantification of viewing strategy, memory and social preferences in rhesus macaques viewing complex social scenes, and they provide an important baseline with which to compare to the effects of therapeutics aimed at enhancing social cognition.
Highlights
Eye tracking has been used to uncover how we explore the visual world and the features that guide our attention
A more sensitive, cluster-based, non-parametric permutation analysis (Maris and Oostenveld, 2007) of fixation duration across time revealed that this effect was specific to the period of 0–4.25 s after stimulus onset when pooling data from all 3 subjects
To date, experiments using social scenes have been limited by potentially confounding variability present in uncontrolled stimuli as well as the extensive time and effort required to draw regions of interest around scene items and analyze the resulting data
Summary
Eye tracking has been used to uncover how we explore the visual world and the features that guide our attention. Subsequent formal analysis revealed that scene exploration begins with long saccades and quick fixations landing on highly informative regions as participants quickly orient to the global gist of the scene, with fixations increasing in duration and saccades decreasing in amplitude as participants focus on local details (Antes, 1974). This early work demonstrated that exploration of the visual world is a dynamic process that changes with experience and is driven by distinguishable features. Amnesic patients with medial temporal lobe damage that includes damage to the hippocampus demonstrate impaired viewing behavior for manipulated scenes (Ryan et al, 2000; Smith et al, 2006; Smith and Squire, 2008)
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