Neural circuit selective for fast but not slow dopamine increases in drug reward

Peter Manza (), Dardo Tomasi, Ehsan Shokri-Kojori, Rui Zhang, Danielle Kroll, Dana Feldman, Katherine McPherson, Catherine Biesecker, Evan Dennis, Allison Johnson, Kai Yuan, Wen-Tung Wang, Michele-Vera Yonga, Gene-Jack Wang and Nora D. Volkow ()
Additional contact information
Peter Manza: National Institutes of Health
Dardo Tomasi: National Institutes of Health
Ehsan Shokri-Kojori: National Institutes of Health
Rui Zhang: National Institutes of Health
Danielle Kroll: National Institutes of Health
Dana Feldman: National Institutes of Health
Katherine McPherson: National Institutes of Health
Catherine Biesecker: National Institutes of Health
Evan Dennis: National Institutes of Health
Allison Johnson: National Institutes of Health
Kai Yuan: Xidian University
Wen-Tung Wang: National Institutes of Health
Michele-Vera Yonga: National Institutes of Health
Gene-Jack Wang: National Institutes of Health
Nora D. Volkow: National Institutes of Health

Nature Communications, 2023, vol. 14, issue 1, 1-11

Abstract: Abstract The faster a drug enters the brain, the greater its addictive potential, yet the brain circuits underlying the rate dependency to drug reward remain unresolved. With simultaneous PET-fMRI we linked dynamics of dopamine signaling, brain activity/connectivity, and self-reported ‘high’ in 20 adults receiving methylphenidate orally (results in slow delivery) and intravenously (results in fast delivery) (trial NCT03326245). We estimated speed of striatal dopamine increases to oral and IV methylphenidate and then tested where brain activity was associated with slow and fast dopamine dynamics (primary endpoint). We then tested whether these brain circuits were temporally associated with individual ‘high’ ratings to methylphenidate (secondary endpoint). A corticostriatal circuit comprising the dorsal anterior cingulate cortex and insula and their connections with dorsal caudate was activated by fast (but not slow) dopamine increases and paralleled ‘high’ ratings. These data provide evidence in humans for a link between dACC/insula activation and fast but not slow dopamine increases and document a critical role of the salience network in drug reward.

Date: 2023
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DOI: 10.1038/s41467-023-41972-6

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