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Neural processing of food and monetary rewards is modulated by metabolic state

Abstract

In humans, food is considered a powerful primary reinforcer, whereas money is a secondary reinforcer, as it gains a value through learning experience. Here, we aimed to identify the neural regions supporting the processing of food-related reinforcers, relate it to the neural underpinnings of monetary reinforcers, and explore their modulation by metabolic state (hunger vs satiety). Twenty healthy male participants were tested in two experimental sessions, once hungry and once satiated, using functional magnetic resonance imaging. Participants performed an associative learning task, receiving food or monetary rewards (in the form of images) on separate blocks. Irrespective of incentive type, both food and monetary rewards engaged ventral striatum, medial orbitofrontal cortex and amygdala, regions that have been previously associated with reward processing. Food incentives additionally engaged the opercular part of the inferior frontal gyrus and the insula, collectively known as a primary gustatory cortex. Moreover, in response to negative feedback (here, reward omission), robust activation was observed in anterior insula, supplementary motor area and lateral parts of the prefrontal cortex, including middle and inferior frontal gyrus. Furthermore, the interaction between metabolic state and incentive type resulted in supramarginal gyrus (SMG) activity, among other motor and sensory-related regions. Finally, functional connectivity analysis showed correlation in the hungry state between the SMG and mesolimbic regions, including the hippocampus, midbrain and cingulate areas. Also, the interaction between metabolic state and incentive type revealed coupling between SMG and ventral striatum. Whereas general purpose reward-related regions process incentives of different kinds, the current results suggest that the SMG might play a key role in integrating the information related to current metabolic state and available incentive type.

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Abbreviations

ANOVA:

Analysis of variance

AROMA:

Automatic Removal of Motion Artifacts

BMI:

Body mass index

DARTEL:

Diffeomorphic anatomical registration through exponentiated lie algebra

FWHM:

Full width half maximum

GLM:

General linear model

ICA:

Independent component analysis

IFG:

Inferior frontal gyrus

IPL:

Inferior parietal lobule

OFC:

Orbitofrontal cortex

PFC:

Prefrontal cortex

SMA:

Supplemental motor area

SMG:

Supramarginal gyrus

VS:

Ventral striatum

VTA:

Ventral tegmental area

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Acknowledgements

The authors do not have any additional financial disclosures. ND, TFM and MH designed research. MY and MG conducted research. MG provided essential support in analysis. MY, MH and ND analyzed data and performed statistical analysis. MY, ND and TFM wrote paper. MY, ND and TFM had primary responsibility for final content.

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Correspondence to Thomas F. Münte.

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The authors have nothing to disclose.

Sources of Support

This work was supported by an intramural grant (E05-2014) of the University of Lübeck to ND and by a grant from the Deutsche Forschungsgemeinschaft (SFB TR134, C01) to TFM. ND is currently an honorary research fellow at the University of Cambridge, funded by the Deutsche Forschungsgemeinschaft (DO1915/1–1).

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Yousuf, M., Heldmann, M., Göttlich, M. et al. Neural processing of food and monetary rewards is modulated by metabolic state. Brain Imaging and Behavior 12, 1379–1392 (2018). https://doi.org/10.1007/s11682-017-9811-y

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  • DOI: https://doi.org/10.1007/s11682-017-9811-y

Keywords

  • Reward
  • Food
  • Money
  • Hunger
  • Satiety
  • Supramarginal gyrus
  • Ventral striatum
  • fMRI