PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging

Angela M. Ianni; Daniel P. Eisenberg; Erie D. Boorman; Sara M. Constantino; Catherine E. Hegarty; Michael D. Gregory; Joseph C. Masdeu; Philip D. Kohn; Timothy E. Behrens; Karen F. Berman

doi:10.1038/s41467-023-41897-0

PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging

Angela M. Ianni, Daniel P. Eisenberg, Erie D. Boorman, Sara M. Constantino, Catherine E. Hegarty, Michael D. Gregory, Joseph C. Masdeu, Philip D. Kohn, Timothy E. Behrens, Karen F. Berman

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Foraging behavior requires weighing costs of time to decide when to leave one reward patch to search for another. Computational and animal studies suggest that striatal dopamine is key to this process; however, the specific role of dopamine in foraging behavior in humans is not well characterized. We use positron emission tomography (PET) imaging to directly measure dopamine synthesis capacity and D₁ and D_2/3 receptor availability in 57 healthy adults who complete a computerized foraging task. Using voxelwise data and principal component analysis to identify patterns of variation across PET measures, we show that striatal D₁ and D_2/3 receptor availability and a pattern of mesolimbic and anterior cingulate cortex dopamine function are important for adjusting the threshold for leaving a patch to explore, with specific sensitivity to changes in travel time. These findings suggest a key role for dopamine in trading reward benefits against temporal costs to modulate behavioral adaptions to changes in the reward environment critical for foraging.

Original language	English (US)
Article number	6122
Pages (from-to)	6122
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-41897-0
State	Published - Sep 30 2023

Keywords

Adult
Animals
Humans
Dopamine
Receptors, Dopamine D2/metabolism
Reward
Corpus Striatum/metabolism
Positron-Emission Tomography/methods

ASJC Scopus subject areas

Physics and Astronomy(all)
Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)

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10.1038/s41467-023-41897-0

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Ianni, A. M., Eisenberg, D. P., Boorman, E. D., Constantino, S. M., Hegarty, C. E., Gregory, M. D., Masdeu, J. C., Kohn, P. D., Behrens, T. E., & Berman, K. F. (2023). PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging. Nature Communications, 14(1), 6122. Article 6122. https://doi.org/10.1038/s41467-023-41897-0

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title = "PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging",

abstract = "Foraging behavior requires weighing costs of time to decide when to leave one reward patch to search for another. Computational and animal studies suggest that striatal dopamine is key to this process; however, the specific role of dopamine in foraging behavior in humans is not well characterized. We use positron emission tomography (PET) imaging to directly measure dopamine synthesis capacity and D1 and D2/3 receptor availability in 57 healthy adults who complete a computerized foraging task. Using voxelwise data and principal component analysis to identify patterns of variation across PET measures, we show that striatal D1 and D2/3 receptor availability and a pattern of mesolimbic and anterior cingulate cortex dopamine function are important for adjusting the threshold for leaving a patch to explore, with specific sensitivity to changes in travel time. These findings suggest a key role for dopamine in trading reward benefits against temporal costs to modulate behavioral adaptions to changes in the reward environment critical for foraging.",

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author = "Ianni, {Angela M.} and Eisenberg, {Daniel P.} and Boorman, {Erie D.} and Constantino, {Sara M.} and Hegarty, {Catherine E.} and Gregory, {Michael D.} and Masdeu, {Joseph C.} and Kohn, {Philip D.} and Behrens, {Timothy E.} and Berman, {Karen F.}",

note = "Funding Information: We thank the participants for choosing to spend their time in service of this work. We are also grateful to the National Institutes of Health Positron Emission Tomography Department for their invaluable help and support. This research was supported by the Intramural Research Program of the National Institute of Health (NIH protocols: NCT00004571, NCT00942981, NCT00024622; funding from NIMH project #: ZIAMH002717, awarded to K.B.). Publisher Copyright: {\textcopyright} 2023, Springer Nature Limited.",

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doi = "10.1038/s41467-023-41897-0",

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AU - Ianni, Angela M.

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AU - Gregory, Michael D.

AU - Masdeu, Joseph C.

AU - Kohn, Philip D.

AU - Behrens, Timothy E.

AU - Berman, Karen F.

N1 - Funding Information: We thank the participants for choosing to spend their time in service of this work. We are also grateful to the National Institutes of Health Positron Emission Tomography Department for their invaluable help and support. This research was supported by the Intramural Research Program of the National Institute of Health (NIH protocols: NCT00004571, NCT00942981, NCT00024622; funding from NIMH project #: ZIAMH002717, awarded to K.B.). Publisher Copyright: © 2023, Springer Nature Limited.

PY - 2023/9/30

Y1 - 2023/9/30

N2 - Foraging behavior requires weighing costs of time to decide when to leave one reward patch to search for another. Computational and animal studies suggest that striatal dopamine is key to this process; however, the specific role of dopamine in foraging behavior in humans is not well characterized. We use positron emission tomography (PET) imaging to directly measure dopamine synthesis capacity and D1 and D2/3 receptor availability in 57 healthy adults who complete a computerized foraging task. Using voxelwise data and principal component analysis to identify patterns of variation across PET measures, we show that striatal D1 and D2/3 receptor availability and a pattern of mesolimbic and anterior cingulate cortex dopamine function are important for adjusting the threshold for leaving a patch to explore, with specific sensitivity to changes in travel time. These findings suggest a key role for dopamine in trading reward benefits against temporal costs to modulate behavioral adaptions to changes in the reward environment critical for foraging.

AB - Foraging behavior requires weighing costs of time to decide when to leave one reward patch to search for another. Computational and animal studies suggest that striatal dopamine is key to this process; however, the specific role of dopamine in foraging behavior in humans is not well characterized. We use positron emission tomography (PET) imaging to directly measure dopamine synthesis capacity and D1 and D2/3 receptor availability in 57 healthy adults who complete a computerized foraging task. Using voxelwise data and principal component analysis to identify patterns of variation across PET measures, we show that striatal D1 and D2/3 receptor availability and a pattern of mesolimbic and anterior cingulate cortex dopamine function are important for adjusting the threshold for leaving a patch to explore, with specific sensitivity to changes in travel time. These findings suggest a key role for dopamine in trading reward benefits against temporal costs to modulate behavioral adaptions to changes in the reward environment critical for foraging.

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PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging

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