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Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

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Abstract

Rationale

Exogenous oxytocin administration is widely reported to improve social cognition in human and nonhuman primate adults. Risk factors of impaired social cognition, however, emerge in infancy. Early interventions—when plasticity is greatest—are critical to reverse negative outcomes.

Objective

We tested the hypothesis that oxytocin may exert similar positive effects on infant social cognition, as in adults. To test this idea, we assessed the effectiveness of acute, aerosolized oxytocin on two foundational social cognitive skills: working memory (i.e., ability to briefly hold and process information) and social gaze (i.e., tracking the direction of others’ gaze) in 1-month-old nursery-reared macaque monkeys (Macaca mulatta). We did not predict sex differences, but we included sex as a factor in our analyses to test whether our effects would be generalizable across both males and females.

Results

In a double-blind, placebo-controlled design, we found that females were more socially skilled at baseline compared to males, and that oxytocin improved working memory and gaze following, but only in males.

Conclusions

These sex differences, while unexpected, may be due to interactions with gonadal steroids and may be relevant to sexually dimorphic disorders of social cognition, such as male-biased autism spectrum disorder, for which oxytocin has been proposed as a potential treatment. In sum, we report the first evidence that oxytocin may influence primate infant cognitive abilities. Moreover, these behavioral effects appear sexually dimorphic, highlighting the importance of considering sex differences. Oxytocin effects observed in one sex may not be generalizable to the other sex.

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Acknowledgements

We thank the staff and researchers in the Laboratory of Comparative Ethology for help with data collection, Paige Fairman for reliability coding, and Sarah E. Maylott for helpful comments. This work was supported by the National Institute of Child Health and Human Development, National Institutes of Health [P01HD064653 to P.F.F.], a James W. McLamore Provost Research Award in Social Sciences, University of Miami [to E.A.S.], and the Division of Intramural Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health.

Author contributions

EAS, AP, VS, and PFF designed the study. SJS provided critical resources. EAS coordinated the study and lead data collection. AP, VS, and SSKK assisted with data collection. EAS coded the videos, analyzed the data, and wrote the manuscript. All authors gave final approval.

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Authors and Affiliations

  1. Department of Psychology, University of Miami, 5665 Ponce De Leon Boulevard, Coral Gables, FL, 33124, USA

    Elizabeth A. Simpson

  2. Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Poolesville, MD, USA

    Elizabeth A. Simpson, Annika Paukner, Valentina Sclafani, Stefano S. K. Kaburu & Stephen J. Suomi

  3. Dipartimento di Neuroscienze, Università di Parma, Parma, Italy

    Elizabeth A. Simpson, Valentina Sclafani, Stefano S. K. Kaburu & Pier F. Ferrari

  4. School of Psychology and Clinical Language Sciences, University of Reading, Reading, UK

    Valentina Sclafani

  5. Department of Population Health and Reproduction, University of California, Davis, CA, USA

    Stefano S. K. Kaburu

  6. Institut des Sciences Cognitives Marc Jeannerod, CNRS / Université Claude Bernard Lyon, Lyon, France

    Pier F. Ferrari

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  1. Elizabeth A. Simpson
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  2. Annika Paukner
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  3. Valentina Sclafani
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  4. Stefano S. K. Kaburu
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  6. Pier F. Ferrari
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Corresponding author

Correspondence to Elizabeth A. Simpson.

Ethics declarations

The Eunice Kennedy Shriver National Institute of Child Health and Human Development Animal Care and Use Committee approved all procedures. The study was conducted in accordance with the Guide for the Care and Use of Laboratory Animals and Complied with the Animal Welfare Act.

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The authors declare that they have no conflicts of interest.

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Simpson, E.A., Paukner, A., Sclafani, V. et al. Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques. Psychopharmacology 234, 497–506 (2017). https://doi.org/10.1007/s00213-016-4480-x

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  • DOI: https://doi.org/10.1007/s00213-016-4480-x

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