Individual differences in scanpaths correspond with serotonin transporter genotype and behavioral phenotype in rhesus monkeys (Macaca mulatta)

Abstract

Scanpaths (the succession of fixations and saccades during spontaneous viewing) contain information about the image but also about the viewer. To determine the viewer-dependent factors in the scanpaths of monkeys, we trained three adult males (Macaca mulatta) to look for 3 s at images of conspecific facial expressions with either direct or averted gaze. The subjects showed significant differences on four basic scanpath parameters (number of fixations, fixation duration, saccade length, and total scanpath length) when viewing the same facial expression/gaze direction combinations. Furthermore, we found differences between monkeys in feature preference and in the temporal order in which features were visited on different facial expressions. Overall, the between-subject variability was larger than the within- subject variability, suggesting that scanpaths reflect individual preferences in allocating visual attention to various features in aggressive, neutral, and appeasing facial expressions. Individual scanpath characteristics were brought into register with the genotype for the serotonin transporter regulatory gene (5-HTTLPR) and with behavioral characteristics such as expression of anticipatory anxiety and impulsiveness/hesitation in approaching food in the presence of a potentially dangerous object.

Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys.

“…Significant differences were observed between the feature preference of the viewers reported here and earlier reports from experiments that used static images of facial expressions (Gibboni, et al, 2009; Gothard, et al, 2004; Keating & Keating, 1982; Nahm, et al, 1997). These differences can be attributed to several factors: (1) only the face is usually presented in static images and not the whole body as in our video segments, (2) in many previous studies monkeys are often required to maintain their gaze on the image for a predefined duration in order to get reward, and/or (3) videos are inherently more salient and the movement alone can “hold” the viewer's attention.…”

“…Monkeys exhibit perceptual bias towards images of their own species (Gothard, Brooks, & Peterson, 2009; Leopold & Rhodes, 2010) and prefer looking at, or interacting with, certain individuals (Deaner, Khera, & Platt, 2005). Based on our previous studies (Gibboni, et al, 2009), that correlated the viewer's 5-HTTLPR genotype, early life experience and other behavioral tendencies with looking patterns or static images we predicted large differences in the subjects' movie viewing preferences.…”

“…Gender, age, social status, and emotional state have been show to contribute to the variability of scanpaths in monkeys (Gibboni, et al, 2009; Klein, Shepherd, & Platt, 2009; Tsuchida & Izumi, 2009) and in humans (e.g., Perlman et al, 2009) In addition to exploring the social determinants of scanpaths, we investigated how socially-triggered looking behaviors varied with the sociability of the viewer monkeys. Monkeys exhibit perceptual bias towards images of their own species (Gothard, Brooks, & Peterson, 2009; Leopold & Rhodes, 2010) and prefer looking at, or interacting with, certain individuals (Deaner, Khera, & Platt, 2005).…”

“…To approximate natural social interactions similar to those documented by field studies, we used unedited video footage to induce in viewer monkeys spontaneous facial expressions and looking patterns in the laboratory setting. Three adult male monkeys, previously behaviorally and genetically (5-HTTLPR) characterized (Gibboni et al, 2009), were monitored while they watched 10 s video segments depicting unfamiliar monkeys (movie monkeys) displaying affiliative, neutral, and aggressive behaviors. The gaze and head orientation of the movie monkeys alternated between ‘averted’ and ‘directed’ at the viewer.…”

The evolution of face processing in primates

“…That said, Gothard et al published a recent study that used eye tracking to specifically address individual differences in face scanning patterns [81]. Using some of the same subjects as in their previous studies, this team presented elegant data showing individual differences in the scan paths made by three monkeys to conspecifics' faces, which correlated with basic behavioural temperament style and serotonin transporter gene polymorphisms [81]. Thus, eye tracking is an extremely rich methodology for studying social cognition and understanding individual differences, but may not be able to differentiate face-processing mechanisms per se.…”