The acute effects of nicotine on corticostriatal responses to distinct phases of reward processing

by | Addiction

https://www.nature.com/articles/s41386-020-0611-5

Comment; In the Nucleus accumbens, nicotine has a stronger effect on anticipation than on outcome.

Neuropsychopharmacology (2020)Cite this article

Abstract

Nicotine enhances the reinforcement of non-drug rewards by increasing nucleus accumbens (NAcc) reactivity to anticipatory cues. This anticipatory effect is selective as no clear evidence has emerged showing that nicotine acutely changes reward receipt reactivity. However, repeated rewarding experiences shift peak brain reactivity from hedonic reward outcome to the motivational anticipatory cue yielding more habitual cue-induced behavior. Given nicotine’s influence on NAcc reactivity and connectivity, it is plausible that nicotine acutely induces this shift and alters NAcc functional connectivity during reward processing. To evaluate this currently untested hypothesis, a randomized crossover design was used in which healthy non-smokers were administered placebo and nicotine (2-mg lozenge). Brain activation to monetary reward anticipation and outcome was evaluated with functional magnetic resonance imaging. Relative to placebo, nicotine induced more NAcc reactivity to reward anticipation. Greater NAcc activation during anticipation was significantly associated with lower NAcc activation to outcome. During outcome, nicotine reduced NAcc functional connectivity with cortical regions including the anterior cingulate cortex, orbitofrontal cortex, and insula. These regions showed the same negative relationship between reward anticipation and outcome as noted in the NAcc. The current findings significantly improve our understanding of how nicotine changes corticostriatal circuit function and communication during distinct phases of reward processing and critically show that these alterations happen acutely following a single dose. The implications of this work explain nicotinic modulation of general reward function, which offer insights into the initial drive to smoke and the subsequent difficulty in cessation.

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Affiliations

  1. McLean Imaging Center, McLean Hospital, Belmont, MA, USA
    • Kainan S. Wang
    • , Maya Zegel
    • , Elena Molokotos
    • , Lauren V. Moran
    • , David P. Olson
    • , Diego A. Pizzagalli
    •  & Amy C. Janes
  2. Harvard Medical School, Boston, MA, USA
    • Kainan S. Wang
    • , Lauren V. Moran
    • , David P. Olson
    • , Diego A. Pizzagalli
    •  & Amy C. Janes
  3. Department of Psychology, Suffolk University, Boston, MA, USA
    • Elena Molokotos

Contributions

A.C.J. conceptualized and designed the study with DAP. M.Z. recruited and collected the data. K.S.W. conducted all analyses and wrote the initial draft with A.C.J. and E.M. L.V.M. and D.O. provided clinical expertise and served as study physicians. All authors reviewed and edited the final manuscript.

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Correspondence to Amy C. Janes.

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Wang, K.S., Zegel, M., Molokotos, E. et al. The acute effects of nicotine on corticostriatal responses to distinct phases of reward processing. Neuropsychopharmacol. (2020) doi:10.1038/s41386-020-0611-5

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