Social relevance drives viewing behavior independent of low-level salience in rhesus macaques

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.

Social targets improve body-based and environment-based strategies during spatial navigation

“…Whereas the bias reduction in experiment 1 may therefore be explained by the general tendency to perceive a person facing oneself as more close than a person looking away (Jung et al 2016), and perhaps as more close than the object used here, there was no bias reduction but still a reduction in position error in experiment 2, which in our view cannot be explained by such a systematic shift towards the self. Our results may therefore indicate a social advantage in spatial encoding, similar as has been observed in other contexts, such as attentional capture for faces (Weaver and Lauwereyns 2011), attentional capture for social stimuli (Gluckman and Johnson 2013), enhanced tactile spatial perception when seeing a hand (Kennett et al 2001), or a social preference when observing complex scenes (Solyst and Buffalo 2014).…”

“…It has been argued before that visual body perception triggers attentional focus (Weaver and Lauwereyns 2011;Gluckman and Johnson 2013;Solyst and Buffalo 2014), perhaps via attentional prioritization (Truong and Todd 2016). Attentional prioritization also modulates hippocampal networks, and the PPC (Cordova et al 2016;Levichkina et al 2017).…”

Human and monkey infant attention to dynamic social and nonsocial stimuli

“…Macaque infants are a promising NHP model, given their similarities with human infants, including strong mother–infant bonds, complex social interactions, and dedicated neural systems for social information processing (Shepherd & Freiwald, 2018). As in humans, adult macaques display privileged processing of social compared to nonsocial stimuli (Machado, Whitaker, Smith, Patterson, & Bauman, 2015; Nakata, Eifuku, & Tamura, 2018; Solyst & Buffalo, 2014; Taubert, Wardle, Flessert, Leopold, & Ungerleider, 2017), and infant macaque social attention is positively correlated with later social development. For example, male infant macaques display an increase social attention between 1 and 6 months of age, especially attention to the eye region of faces, and this increase is associated with more prosocial peer interactions between 3 and 18 months of age (Ryan et al., in press).…”

Preferential Processing of Social Features and Their Interplay with Physical Saliency in Complex Naturalistic Scenes

“…Importantly, prior research also shed light on the power of saliency-based predictions in the context of social information. For example, several studies yielded support that the influence of physical saliency on gazing behavior may be especially weak for socially relevant stimuli (e.g., Nyström and Holmqvist, 2008; Birmingham et al, 2009a,b; Fletcher-Watson et al, 2009; Zwickel and Vo, 2010; Hall et al, 2011; Scheller et al, 2012; Suda and Kitazawa, 2015; see also Kano and Tomonaga, 2011; Solyst and Buffalo, 2014) and a number of modeling approaches provided evidence that further sources of information (e.g., locations of faces) may be considered in addition to low-level saliency (e.g., Cerf et al, 2008, 2009; Marat et al, 2013; Xu et al, 2014; Parks et al, 2015; for a review, see Tatler et al, 2011). However, the attentional influence of physical saliency in the context of social information has so far not been characterized sufficiently.…”