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Research Articles, Behavioral/Cognitive

Increasing Central Serotonin with 5-hydroxytryptophan Disrupts the Inhibition of Social Gaze in Nonhuman Primates

Hannah B. Weinberg-Wolf, Nick Fagan, Olga Dal Monte and Steve W. C. Chang
Journal of Neuroscience 26 January 2022, 42 (4) 670-681; DOI: https://doi.org/10.1523/JNEUROSCI.0413-21.2021
Hannah B. Weinberg-Wolf
1Department of Psychology, Yale University, New Haven, Connecticut 06520
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Nick Fagan
1Department of Psychology, Yale University, New Haven, Connecticut 06520
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Olga Dal Monte
1Department of Psychology, Yale University, New Haven, Connecticut 06520
2Department of Psychology, University of Turin, 10124 Turin, Italy
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Steve W. C. Chang
1Department of Psychology, Yale University, New Haven, Connecticut 06520
3Department of Neuroscience, Yale University School of Medicine, New Haven, Connecticut 06510
4Kavli Institute for Neuroscience, Yale University School of Medicine, New Haven, Connecticut 06510
5Wu Tsai Institute, Yale University, New Haven, Connecticut 06510
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Abstract

To competently navigate the world, individuals must flexibly balance distinct aspects of social gaze, orienting toward others and inhibiting orienting responses, depending on the context. These behaviors are often disrupted amongst patient populations treated with serotonergic drugs. However, those in the field lack a clear understanding of how the serotonergic system mediates social orienting and inhibiting behaviors. Here, we tested how increasing central concentrations of serotonin with the direct precursor 5-hydroxytryptophan (5-HTP) would modulate the ability of rhesus macaques (both sexes) to use eye movements to flexibly orient to, or inhibit orienting to, faces. Systemic administrations of 5-HTP effectively increased central serotonin levels and impaired flexible orientation and inhibition. Critically, 5-HTP selectively impaired the ability of monkeys to inhibit orienting to face images, whereas it similarly impaired orienting to face and control images. 5-HTP also caused monkeys to perseverate on their gaze responses, making them worse at flexibly switching between orienting and inhibiting behaviors. Furthermore, the effects of 5-HTP on performance correlated with a constriction of the pupil, an increased time to initiate trials, and an increased reaction time, suggesting that the disruptive effects of 5-HTP on social gaze behaviors are likely driven by a downregulation of arousal and motivational states. Together, these findings provide causal evidence for a modulatory relationship between 5-HTP and social gaze behaviors in nonhuman primates and offer translational insights for the role of the serotonergic system in social gaze.

SIGNIFICANCE STATEMENT Behavioral changes arising from pharmacological agents that target serotonergic functions are complex and difficult to predict. Here, we examined the causal impacts of administering the direct precursor of serotonin, 5-HTP, on orienting and inhibiting social gaze in nonhuman primates. 5-HTP increased central concentrations of serotonin and selectively impaired the ability of monkeys to inhibit orienting to faces while similarly impairing the ability of monkeys to orient to face and control images. These behavioral gaze impairments were systematically associated with a downregulation of arousal and motivational states, indexed by pupil constriction, increased time to initiate trials, and increased reaction time. These findings provide a causal link between 5-HTP and social gaze behaviors in nonhuman primates and provide translational insights about serotonergic interventions.

  • 5-HTP
  • causal impairment
  • gaze inhibition
  • gaze orientation
  • nonhuman primates
  • serotonin

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The Journal of Neuroscience: 42 (4)
Journal of Neuroscience
Vol. 42, Issue 4
26 Jan 2022
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Increasing Central Serotonin with 5-hydroxytryptophan Disrupts the Inhibition of Social Gaze in Nonhuman Primates
Hannah B. Weinberg-Wolf, Nick Fagan, Olga Dal Monte, Steve W. C. Chang
Journal of Neuroscience 26 January 2022, 42 (4) 670-681; DOI: 10.1523/JNEUROSCI.0413-21.2021

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Increasing Central Serotonin with 5-hydroxytryptophan Disrupts the Inhibition of Social Gaze in Nonhuman Primates
Hannah B. Weinberg-Wolf, Nick Fagan, Olga Dal Monte, Steve W. C. Chang
Journal of Neuroscience 26 January 2022, 42 (4) 670-681; DOI: 10.1523/JNEUROSCI.0413-21.2021
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Keywords

  • 5-HTP
  • causal impairment
  • gaze inhibition
  • gaze orientation
  • nonhuman primates
  • serotonin

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