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High-intensity sweet taste as a predictor of subjective alcohol responses to the ascending limb of an intravenous alcohol prime: an fMRI study

Neuropsychopharmacology volume 49, pages 396–404 (2024)Cite this article

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A Correction to this article was published on 28 August 2023

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Abstract

High-intensity sweet-liking has been linked to alcohol use disorder (AUD) risk. However, the neural underpinning of this association is poorly understood. To find a biomarker predictive of AUD, 140 participants (social and heavy drinkers, ages 21–26) underwent functional magnetic resonance imaging (fMRI) during a monetary incentive delay (MID) task and stimulation with high (SucroseHigh)- and low-concentration sucrose, as well as viscosity-matched water. On another day after imaging, and just before free-access intravenous alcohol self-administration, participants experienced a 30 mg% alcohol prime (10 min ascent) using the Computerized Alcohol Infusion System. Principal component analysis (PCA) of subjective responses (SR) to the prime’s ascending limb generated enjoyable (SRenjoy) and sedative (SRsed) intoxication components. Another PCA created one component reflective of self-administered alcohol exposure (AE) over 90 min. Component loadings were entered as regressors in a voxel-wise general linear fMRI model, with reward type as a fixed factor. By design, peak prime breath alcohol concentration was similar across participants (29 ± 3.4 mg%). SRenjoy on the prime’s ascending limb correlated positively with [SucroseHigh > Water] in the supplementary motor area and right dorsal anterior insula, implicating the salience network. Neither SR component correlated with the brain’s response to MID. AE was unrelated to brain reward activation. While these findings do not support a relationship between alcohol self-administration and (1) subjective liking of or (2) regional brain response to an intensely sweet taste, they show that alcohol’s enjoyable intoxicating effects on the rising limb correspond with anterior insular and supplementary motor area responses to high-concentration sucrose taste. No such associations were observed with MID despite robust activation in those regions. Insula and supplementary motor area responses to intense sensations relate to a known risk factor for AUD in a way that is not apparent with a secondary (monetary) reward.

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Fig. 1: BOLD activation from high-concentration sucrose (SucroseHigh) compared to water in the supplementary motor area and dorsal anterior insula correlates positively with subjective ratings of the enjoyable intoxicating effects of a fixed exposure to intravenous ethanol.
Fig. 2: BOLD activation to [SucroseHigh > Water] and MID cued anticipation, as well as their conjunction (∩), show similar activation of the supplementary motor area (SMA) and the dorsal anterior insula (daINS).
Fig. 3: Correlations between enjoyable intoxication from alcohol and response to supplementary motor area (SMA, top) and dorsal anterior insula (daINS, bottom) BOLD activation from high-concentration sucrose ([SucroseHigh > Water], black triangles, left) and high monetary reward ([Win5 > Neutral]cue and [Win5 > Neutral]feedback; red circles) vs their respective controls, with monetary reward contrasts at the times of reward cues (center) and feedback (right).

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Acknowledgements

The authors gratefully acknowledge Azziza Ahdoot, Rachel Baum, Paige Erb, Tetlu Myint, Caron Peper, Kathryn Snyder, Christina Souert, Shreya Patel. Dr. Claire Carron, and Cari Tsinovoi for subject recruiting and management, Drs. Sarine Janetsian-Fritz and William J.A. Eiler for intellectual contributions to previous iterations of this project, Dr. Yu-Chien Wu, Dr. Sourajit Mustafi, Michele Dragoo, Traci Day, and Robert Bryant Jr. for technical assistance with MRI, Keegan Sawin and Hannah Marotta for assistance with data management and study day expertise, and Dwight Hector, Ph.D. for design refinements and construction of the gustometer. We further thank Dr. Brian Knutson for permitting us the use of his monetary incentive delay task as well as Dr. James Bjork for early discussions on its use.

Funding

This work was supported by an NIAAA fellowship T32 AA07462 to JPA, and by R01 AA022476, P60 AA007611 to DAK.

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Author notes

  1. Katherine Benson

    Present address: Clinical Psychology Graduate Program, Department of Psychology and Neuroscience, University of North Carolina- Chapel Hill, Chapel Hill, NC, USA

  2. George Chittum

    Present address: Department of Pharmacology & Toxicology, Indiana University School of Medicine, Indianapolis, IN, USA

Authors and Affiliations

  1. Medical Neuroscience Graduate Program, Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA

    Jonathan Alessi

  2. Indiana Alcohol Research Center, Indiana University School of Medicine, Indianapolis, IN, USA

    Mario Dzemidzic, Ann Kosobud, Jaroslaw Harezlak, Martin H. Plawecki, Sean J. O’Connor & David A. Kareken

  3. Department of Neurology, Indiana University School of Medicine, Indianapolis, IN, USA

    Mario Dzemidzic, Katherine Benson, George Chittum, Ann Kosobud, Martin H. Plawecki, Sean J. O’Connor & David A. Kareken

  4. Department of Radiology, Indiana University School of Medicine, Indianapolis, IN, USA

    Mario Dzemidzic & David A. Kareken

  5. Department of Epidemiology and Biostatistics, Indiana University School of Public Health, Bloomington, IN, USA

    Jaroslaw Harezlak

  6. Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, USA

    Martin H. Plawecki, Sean J. O’Connor & David A. Kareken

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Contributions

The authors confirm contribution to the paper as follows: study conception and design: DAK, MD, JH, SJO’C, AEKK; data collection: GC, KB; analysis and interpretation of results: JPA, DAK, MD, GC, KB. Draft manuscript preparation: JPA, MD, DAK. All authors reviewed the results and approved the final version of the manuscript.

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The original online version of this article was revised: the publication date for reference 21 was corrected from 2016 to 1977. The correct reference should read “Radloff LS. The CES-D Scale. Appl Psychol Meas. 1977;1:385–401”.

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Alessi, J., Dzemidzic, M., Benson, K. et al. High-intensity sweet taste as a predictor of subjective alcohol responses to the ascending limb of an intravenous alcohol prime: an fMRI study. Neuropsychopharmacol. 49, 396–404 (2024). https://doi.org/10.1038/s41386-023-01684-3

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