Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange

Seth R Batten; Dan Bang; Brian H Kopell; Arianna N Davis; Matthew Heflin; Qixiu Fu; Ofer Perl; Kimia Ziafat; Alice Hashemi; Ignacio Saez; Leonardo S Barbosa; Thomas Twomey; Terry Lohrenz; Jason P White; Peter Dayan; Alexander W Charney; Martijn Figee; Helen S Mayberg; Kenneth T Kishida; Xiaosi Gu; P Read Montague

doi:10.1038/s41562-024-01831-w

Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange

Seth R Batten, Dan Bang, Brian H Kopell, Arianna N Davis, Matthew Heflin, Qixiu Fu, Ofer Perl, Kimia Ziafat, Alice Hashemi, Ignacio Saez, Leonardo S Barbosa, Thomas Twomey, Terry Lohrenz, Jason P White, Peter Dayan, Alexander W Charney, Martijn Figee, Helen S Mayberg, Kenneth T Kishida, Xiaosi GuP Read Montague

Department of Clinical Medicine - Center of Functionally Integrative Neuroscience

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

6 Citations (Scopus)

Abstract

Dopamine and serotonin are hypothesized to guide social behaviours. In humans, however, we have not yet been able to study neuromodulator dynamics as social interaction unfolds. Here, we obtained subsecond estimates of dopamine and serotonin from human substantia nigra pars reticulata during the ultimatum game. Participants, who were patients with Parkinson's disease undergoing awake brain surgery, had to accept or reject monetary offers of varying fairness from human and computer players. They rejected more offers in the human than the computer condition, an effect of social context associated with higher overall levels of dopamine but not serotonin. Regardless of the social context, relative changes in dopamine tracked trial-by-trial changes in offer value-akin to reward prediction errors-whereas serotonin tracked the current offer value. These results show that dopamine and serotonin fluctuations in one of the basal ganglia's main output structures reflect distinct social context and value signals.

Original language	English
Journal	Nature Human Behaviour
Volume	8
Issue	4
Pages (from-to)	718-728
Number of pages	11
ISSN	2397-3374
DOIs	https://doi.org/10.1038/s41562-024-01831-w
Publication status	Published - Apr 2024

Keywords

Aged
Dopamine/metabolism
Female
Humans
Male
Middle Aged
Parkinson Disease/metabolism
Reward
Serotonin/metabolism
Social Behavior
Substantia Nigra/metabolism

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Batten, S. R., Bang, D., Kopell, B. H., Davis, A. N., Heflin, M., Fu, Q., Perl, O., Ziafat, K., Hashemi, A., Saez, I., Barbosa, L. S., Twomey, T., Lohrenz, T., White, J. P., Dayan, P., Charney, A. W., Figee, M., Mayberg, H. S., Kishida, K. T., ... Montague, P. R. (2024). Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange. Nature Human Behaviour, 8(4), 718-728. https://doi.org/10.1038/s41562-024-01831-w

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abstract = "Dopamine and serotonin are hypothesized to guide social behaviours. In humans, however, we have not yet been able to study neuromodulator dynamics as social interaction unfolds. Here, we obtained subsecond estimates of dopamine and serotonin from human substantia nigra pars reticulata during the ultimatum game. Participants, who were patients with Parkinson's disease undergoing awake brain surgery, had to accept or reject monetary offers of varying fairness from human and computer players. They rejected more offers in the human than the computer condition, an effect of social context associated with higher overall levels of dopamine but not serotonin. Regardless of the social context, relative changes in dopamine tracked trial-by-trial changes in offer value-akin to reward prediction errors-whereas serotonin tracked the current offer value. These results show that dopamine and serotonin fluctuations in one of the basal ganglia's main output structures reflect distinct social context and value signals.",

keywords = "Aged, Dopamine/metabolism, Female, Humans, Male, Middle Aged, Parkinson Disease/metabolism, Reward, Serotonin/metabolism, Social Behavior, Substantia Nigra/metabolism",

author = "Batten, {Seth R} and Dan Bang and Kopell, {Brian H} and Davis, {Arianna N} and Matthew Heflin and Qixiu Fu and Ofer Perl and Kimia Ziafat and Alice Hashemi and Ignacio Saez and Barbosa, {Leonardo S} and Thomas Twomey and Terry Lohrenz and White, {Jason P} and Peter Dayan and Charney, {Alexander W} and Martijn Figee and Mayberg, {Helen S} and Kishida, {Kenneth T} and Xiaosi Gu and Montague, {P Read}",

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year = "2024",

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doi = "10.1038/s41562-024-01831-w",

language = "English",

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Batten, SR, Bang, D, Kopell, BH, Davis, AN, Heflin, M, Fu, Q, Perl, O, Ziafat, K, Hashemi, A, Saez, I, Barbosa, LS, Twomey, T, Lohrenz, T, White, JP, Dayan, P, Charney, AW, Figee, M, Mayberg, HS, Kishida, KT, Gu, X & Montague, PR 2024, 'Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange', Nature Human Behaviour, vol. 8, no. 4, pp. 718-728. https://doi.org/10.1038/s41562-024-01831-w

Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange. / Batten, Seth R; Bang, Dan; Kopell, Brian H et al.
In: Nature Human Behaviour, Vol. 8, No. 4, 04.2024, p. 718-728.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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T1 - Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange

AU - Batten, Seth R

AU - Bang, Dan

AU - Kopell, Brian H

AU - Davis, Arianna N

AU - Heflin, Matthew

AU - Fu, Qixiu

AU - Perl, Ofer

AU - Ziafat, Kimia

AU - Hashemi, Alice

AU - Saez, Ignacio

AU - Barbosa, Leonardo S

AU - Twomey, Thomas

AU - Lohrenz, Terry

AU - White, Jason P

AU - Dayan, Peter

AU - Charney, Alexander W

AU - Figee, Martijn

AU - Mayberg, Helen S

AU - Kishida, Kenneth T

AU - Gu, Xiaosi

AU - Montague, P Read

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N2 - Dopamine and serotonin are hypothesized to guide social behaviours. In humans, however, we have not yet been able to study neuromodulator dynamics as social interaction unfolds. Here, we obtained subsecond estimates of dopamine and serotonin from human substantia nigra pars reticulata during the ultimatum game. Participants, who were patients with Parkinson's disease undergoing awake brain surgery, had to accept or reject monetary offers of varying fairness from human and computer players. They rejected more offers in the human than the computer condition, an effect of social context associated with higher overall levels of dopamine but not serotonin. Regardless of the social context, relative changes in dopamine tracked trial-by-trial changes in offer value-akin to reward prediction errors-whereas serotonin tracked the current offer value. These results show that dopamine and serotonin fluctuations in one of the basal ganglia's main output structures reflect distinct social context and value signals.

AB - Dopamine and serotonin are hypothesized to guide social behaviours. In humans, however, we have not yet been able to study neuromodulator dynamics as social interaction unfolds. Here, we obtained subsecond estimates of dopamine and serotonin from human substantia nigra pars reticulata during the ultimatum game. Participants, who were patients with Parkinson's disease undergoing awake brain surgery, had to accept or reject monetary offers of varying fairness from human and computer players. They rejected more offers in the human than the computer condition, an effect of social context associated with higher overall levels of dopamine but not serotonin. Regardless of the social context, relative changes in dopamine tracked trial-by-trial changes in offer value-akin to reward prediction errors-whereas serotonin tracked the current offer value. These results show that dopamine and serotonin fluctuations in one of the basal ganglia's main output structures reflect distinct social context and value signals.

KW - Aged

KW - Dopamine/metabolism

KW - Female

KW - Humans

KW - Male

KW - Middle Aged

KW - Parkinson Disease/metabolism

KW - Reward

KW - Serotonin/metabolism

KW - Social Behavior

KW - Substantia Nigra/metabolism

U2 - 10.1038/s41562-024-01831-w

DO - 10.1038/s41562-024-01831-w

M3 - Journal article

C2 - 38409356

SN - 2397-3374

VL - 8

SP - 718

EP - 728

JO - Nature Human Behaviour

JF - Nature Human Behaviour

IS - 4

ER -

Dopamine and serotonin in human substantia nigra track social context and value signals during economic exchange

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Keywords

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