Direct serotonin release in humans shapes aversive learning and inhibition

Michael J. Colwell (), Hosana Tagomori, Fei Shang, Hoi Iao Cheng, Chloe E. Wigg, Michael Browning, Philip J. Cowen, Susannah E. Murphy and Catherine J. Harmer ()
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Michael J. Colwell: University of Oxford, Warneford Hospital
Hosana Tagomori: University of Oxford, Warneford Hospital
Fei Shang: University of Oxford, Warneford Hospital
Hoi Iao Cheng: University of Oxford, Warneford Hospital
Chloe E. Wigg: University of Oxford, Warneford Hospital
Michael Browning: University of Oxford, Warneford Hospital
Philip J. Cowen: University of Oxford, Warneford Hospital
Susannah E. Murphy: University of Oxford, Warneford Hospital
Catherine J. Harmer: University of Oxford, Warneford Hospital

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract The role of serotonin in human behaviour is informed by approaches which allow in vivo modification of synaptic serotonin. However, characterising the effects of increased serotonin signalling in human models of behaviour is challenging given the limitations of available experimental probes, notably selective serotonin reuptake inhibitors. Here we use a now-accessible approach to directly increase synaptic serotonin in humans (a selective serotonin releasing agent) and examine its influence on domains of behaviour historically considered core functions of serotonin. Computational techniques, including reinforcement learning and drift diffusion modelling, explain participant behaviour at baseline and after week-long intervention. Reinforcement learning models reveal that increasing synaptic serotonin reduces sensitivity for outcomes in aversive contexts. Furthermore, increasing synaptic serotonin enhances behavioural inhibition, and shifts bias towards impulse control during exposure to aversive emotional probes. These effects are seen in the context of overall improvements in memory for neutral verbal information. Our findings highlight the direct effects of increasing synaptic serotonin on human behaviour, underlining its role in guiding decision-making within aversive and more neutral contexts, and offering implications for longstanding theories of central serotonin function.

Date: 2024
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DOI: 10.1038/s41467-024-50394-x

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