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

Nat Commun. 2023 Sep 30;14(1):6122. doi: 10.1038/s41467-023-41897-0.

Authors

Angela M Ianni^{1

2

3}, Daniel P Eisenberg⁴, Erie D Boorman⁵, Sara M Constantino^{6

7

8

9}, Catherine E Hegarty⁴, Michael D Gregory⁴, Joseph C Masdeu^{4

10

11}, Philip D Kohn⁴, Timothy E Behrens^#⁵, Karen F Berman^#⁴

Affiliations

¹ Clinical & Translational Neuroscience Branch, National Institutes of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD, USA. ianniam@upmc.edu.
² Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom. ianniam@upmc.edu.
³ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA. ianniam@upmc.edu.
⁴ Clinical & Translational Neuroscience Branch, National Institutes of Mental Health, Intramural Research Program, National Institutes of Health, Bethesda, MD, USA.
⁵ Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, United Kingdom.
⁶ Department of Psychology, New York University, New York, NY, USA.
⁷ School of Public Policy and Urban Affairs, Northeastern University, Boston, MA, USA.
⁸ Department of Psychology, Northeastern University, Boston, MA, USA.
⁹ School of Public and International Affairs, Princeton University, Princeton, NJ, USA.
¹⁰ Houston Methodist Institute for Academic Medicine, Houston, TX, USA.
¹¹ Weill Cornell Medicine, New York, NY, USA.

^# Contributed equally.

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.

Trial registration: ClinicalTrials.gov NCT00004571 NCT00942981 NCT00024622.

Publication types

Research Support, N.I.H., Intramural

MeSH terms

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

Substances

Dopamine
Receptors, Dopamine D2

Associated data

ClinicalTrials.gov/NCT00004571
ClinicalTrials.gov/NCT00942981
ClinicalTrials.gov/NCT00024622

Grants and funding

ZIA MH002717/ImNIH/Intramural NIH HHS/United States