Dopamine and Serotonin in Human Substantia Nigra Track Social Context and Value Signals During Economic Exchange
Background Introduction
In contemporary neuroscience research, dopamine and serotonin are hypothesized to be crucial neuromodulators guiding social behavior. However, there is a significant lack of understanding regarding the dynamic changes of these neuromodulators during social interactions. Although non-invasive functional neuroimaging methods (such as EEG and fMRI) have helped to map the “social brain” network related to social tasks in the brain, these methods often face trade-offs in spatial and temporal resolutions, and the obtained data reflect a mix of electrical and chemical events. Therefore, our understanding of the human social brain at a finer biological scale remains insufficient.
The research team proposed a new electrochemical method capable of detecting fluctuations of dopamine and serotonin in the human brain at a millisecond level. Previous studies have shown that dopamine and serotonin play a key role in reward prediction errors and adaptive behaviors in mice, but animal models still cannot fully represent the complexity of human social interactions.
Research Source
This paper was co-authored by Seth R. Batten, Dan Bang, Brian H. Kopell, and others. The research team comes from multiple institutions, including Virginia Tech, Oxford University, Aarhus University, and the Icahn School of Medicine at Mount Sinai. The article was published in the April 2024 issue of Nature Human Behaviour.
Research Workflow
Subjects and Procedure
The subjects were four patients with Parkinson’s disease who acted as participants during deep brain stimulation (DBS) surgeries and played the Ultimatum Game. During the experiment, researchers used an electrochemical method with carbon fiber electrodes to continuously obtain data on dopamine and serotonin fluctuations in the brain’s Substantia Nigra Pars Reticulata (SNR).
The experiment involved two surgeries, spaced 14 to 28 days apart. In each surgery, participants played the Ultimatum Game with a computer or another person, performing 60 trials in total (30 trials per condition). The experiment adopted a crossover balanced design, with each condition blocked within one session.
Data Collection and Analysis
Researchers used a fast-scan cyclic voltammetry (FSCV) electrochemical method to acquire 10 samples of dopamine and serotonin data per second. By inserting carbon fiber electrodes into deep brain structures and conducting electrochemical recordings during experimental tasks, the research team was able to capture rapid fluctuations of neuromodulators during social tasks.
To accurately predict the concentrations of neuromodulators, the team developed a signal prediction model. This model was trained using machine learning methods on a large laboratory dataset to achieve high precision and sensitivity in predicting in vivo data. Non-training data were used in model evaluation, demonstrating its efficiency and accuracy.
Main Findings and Contributions
Behavioral Results
The experimental results showed that participants refused proposals more frequently when they were made by humans (50% of proposals were accepted under the human condition, while 75% were accepted under the computer condition). It was found that the condition significantly influenced the choices, and the overall level of dopamine significantly increased when facing proposals made by humans.
Fluctuations of Neuromodulators
In the neuromodulator data from the experiment, researchers found that changes in dopamine relative to the baseline were closely related to changes in the proposal value (relative to the previous proposal); serotonin, on the other hand, tracked the absolute value of the current proposal, irrespective of the previous proposals.
Research Conclusion
In summary, the research results indicate that dopamine and serotonin not only support value computation but also use these statistics based on norms during social interactions. Changes in dopamine reflect reward prediction error (RPE), corresponding to the difference in the value of the current and previous proposals, while changes in serotonin are related to the absolute value of the current proposal.
Significance and Value of the Research
This study provides the first direct evidence of rapid fluctuations of dopamine and serotonin in the human brain during social interactions. The results suggest that these two neuromodulators play complementary roles in value computation and norm-driven social behavior, which is crucial for understanding the role of fast neuromodulator signals in social behavior.
Research Highlights
Innovative Experimental Method: By using electrochemical methods during DBS surgery, real-time fluctuation data of dopamine and serotonin in the human brain were captured.
Discovery of Dopamine’s Relationship with Social Contexts: Dopamine levels significantly increased when facing proposals made by humans, indicating its role in social fairness perception.
Revealing Complementary Roles of Dopamine and Serotonin: Dopamine rapidly responds to value changes, while serotonin tracks the current value, revealing their complementary functions in value encoding.
Through this study, we not only expanded the understanding of dopamine and serotonin in social behavior but also provided new research methods and analytical frameworks that are valuable references and inspirations for future neuroscience research.