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      Non-invasive Eye Tracking Methods for New World and Old World Monkeys

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          Abstract

          Eye-tracking methods measure what humans and other animals visually attend to in the environment. In nonhuman primates, eye tracking can be used to test hypotheses about how primates process social information. This information can further our understanding of primate behavior as well as offer unique translational potential to explore causes of or treatments for altered social processing as seen in people with neurodevelopmental disorders such as autism spectrum disorder and schizophrenia. However, previous methods for collecting eye-tracking data in nonhuman primates required some form of head restraint, which limits the opportunities for research with respect to the number of or kinds of primates that can undergo an eye-tracking study. We developed a novel, noninvasive method for collecting eye tracking data that can be used both in animals that are difficult to restrain without sedation as well as animals that are of different ages and sizes as the box size can be adjusted. Using a transport box modified with a viewing window, we collected eye-tracking data in both New ( Callicebus cupreus) and Old World monkeys ( Macaca mulatta) across multiple developmental time points. These monkeys had the option to move around the box and avert their eyes from the screen, yet, they demonstrated a natural interest in viewing species-specific imagery with no previous habituation to the eye-tracking paradigm. Provided with opportunistic data from voluntary viewing of stimuli, we found that juveniles viewed stimuli more than other age groups, videos were viewed more than static photo imagery, and that monkeys increased their viewing time when presented with multiple eye tracking sessions. This noninvasive approach opens new opportunities to integrate eye-tracking studies into nonhuman primate research.

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          Most cited references46

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          What is "special" about face perception?

          There is growing evidence that face recognition is "special" but less certainty concerning the way in which it is special. The authors review and compare previous proposals and their own more recent hypothesis, that faces are recognized "holistically" (i.e., using relatively less part decomposition than other types of objects). This hypothesis, which can account for a variety of data from experiments on face memory, was tested with 4 new experiments on face perception. A selective attention paradigm and a masking paradigm were used to compare the perception of faces with the perception of inverted faces, words, and houses. Evidence was found of relatively less part-based shape representation for faces. The literatures on machine vision and single unit recording in monkey temporal cortex are also reviewed for converging evidence on face representation. The neuropsychological literature is reviewed for-evidence on the question of whether face representation differs in degree or kind from the representation of other types of objects.
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            Activation of the maternal immune system during pregnancy alters behavioral development of rhesus monkey offspring.

            Maternal infection during pregnancy is associated with an increased risk of schizophrenia and autism in the offspring. Supporting this correlation, experimentally activating the maternal immune system during pregnancy in rodents produces offspring with abnormal brain and behavioral development. We have developed a nonhuman primate model to bridge the gap between clinical populations and rodent models of maternal immune activation (MIA). A modified form of the viral mimic, synthetic double-stranded RNA (polyinosinic:polycytidylic acid stabilized with poly-L-lysine) was delivered to two separate groups of pregnant rhesus monkeys to induce MIA: 1) late first trimester MIA (n = 6), and 2) late second trimester MIA (n = 7). Control animals (n = 11) received saline injections at the same first or second trimester time points or were untreated. Sickness behavior, temperature, and cytokine profiles of the pregnant monkeys confirmed a strong inflammatory response to MIA. Behavioral development of the offspring was studied for 24 months. Following weaning at 6 months of age, MIA offspring exhibited abnormal responses to separation from their mothers. As the animals matured, MIA offspring displayed increased repetitive behaviors and decreased affiliative vocalizations. When evaluated with unfamiliar conspecifics, first trimester MIA offspring deviated from species-typical macaque social behavior by inappropriately approaching and remaining in immediate proximity of an unfamiliar animal. In this rhesus monkey model, MIA yields offspring with abnormal repetitive behaviors, communication, and social interactions. These results extended the findings in rodent MIA models to more human-like behaviors resembling those in both autism and schizophrenia. Copyright © 2014 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
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              A Meta-Analysis of Gaze Differences to Social and Nonsocial Information Between Individuals With and Without Autism.

              Numerous studies have identified abnormal gaze in individuals with autism. However, only some findings have been replicated, the magnitude of effects is unclear, and the pattern of gaze differences across stimuli remains poorly understood. To address these gaps, a comprehensive meta-analysis of autism eye-tracking studies was conducted.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                05 March 2019
                2019
                : 13
                : 39
                Affiliations
                [1] 1The UC Davis MIND Institute, University of California , Davis, Sacramento, CA, United States
                [2] 2Department of Psychiatry and Behavioral Sciences, University of California , Davis, Sacramento, CA, United States
                [3] 3California National Primate Research Center, University of California, Davis , Davis, CA, United States
                [4] 4Department of Psychology, University of California, Davis , Davis, CA, United States
                [5] 5Platform Technology Research Unit, Drug Research Division, Sumitomo Dainippon Pharma Co., Ltd. , Osaka, Japan
                Author notes

                Edited by: Carlos Tomaz, Universidade Ceuma, Brazil

                Reviewed by: Hisao Nishijo, University of Toyama, Japan; Konstantinos Hadjidimitrakis, Monash University, Australia

                *Correspondence: Melissa D. Bauman, mdbauman@ 123456ucdavis.edu

                These authors have contributed equally to this work as first authors

                These authors have contributed equally to this work as last authors

                Article
                10.3389/fnbeh.2019.00039
                6412371
                7e823256-07db-493b-8559-d08710e4f858
                Copyright © 2019 Ryan, Freeman, Murai, Lau, Palumbo, Hogrefe, Bales and Bauman.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 November 2018
                : 14 February 2019
                Page count
                Figures: 7, Tables: 1, Equations: 0, References: 54, Pages: 10, Words: 0
                Funding
                Funded by: Eunice Kennedy Shriver National Institute of Child Health and Human Development 10.13039/100009633
                Funded by: National Institutes of Health 10.13039/100000002
                Categories
                Neuroscience
                Methods

                Neurosciences
                eye tracking,nonhuman primate,rhesus macaque,titi monkey,social neuroscience
                Neurosciences
                eye tracking, nonhuman primate, rhesus macaque, titi monkey, social neuroscience

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