Cited by 25Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesMemory and Neural Mechanisms

Anticipation of Appetitive Operant Action Induces Sustained Dopamine Release in the Nucleus Accumbens

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Goedhoop, Jessica, Arbab, Tara, Willuhn, Ingo·2023·The Journal of Neuroscience

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Abstract

ABSTRACT The mesolimbic dopamine system is implicated in signaling reward-related information as well as in actions that generate rewarding outcomes. These implications are commonly investigated in either Pavlovian or operant reinforcement paradigms, where only the latter requires instrumental action. To parse contributions of reward- and action-related information to dopamine signals, we directly compared the two paradigms: rats underwent either Pavlovian or operant conditioning while dopamine release was measured in the nucleus accumbens, a brain region central for processing this information. Task conditions were identical with the exception of the operant-lever response requirement. Rats in both groups released the same quantity of dopamine at the onset of the reward-predictive cue. However, only the operant-conditioning group showed a subsequent, sustained plateau in dopamine concentration throughout the entire five-second cue presentation (preceding the required action). This dopamine “ramp” was unaffected by probabilistic reward delivery, occurred exclusively prior to operant actions, and was not related to task performance or task acquisition, as it persisted throughout the two-week daily behavioral training. Instead, the ramp flexibly increased in duration with longer cue presentation, seemingly modulating the initial cue-onset triggered dopamine release (i.e., the reward-prediction error (RPE) signal), as both signal amplitude and sustain diminished when reward timing was made more predictable. Thus, our findings suggest that RPE and action components of dopamine release can be differentiated temporally into phasic and ramping/sustained signals, respectively, where the latter depends on the former and presumably reflects the anticipation or incentivization of appetitive action, conceptually akin to motivation. Significance Statement It is unclear whether the components of dopamine signals that are related to reward-associated information and reward-driven approach behavior can be separated. Most studies investigating the dopamine system utilize either Pavlovian or operant conditioning, which both involve the delivery of reward and necessitate appetitive approach behavior. Thus, used exclusively, neither paradigm can disentangle the contributions of these components to dopamine release. However, by combining both paradigms in the same study, we find that anticipation of a reward-driven operant action induces a modulation of reward-prediction-associated dopamine release, producing so-called “dopamine ramps”. Therefore, our findings provide new insight into dopamine ramps, and suggest that dopamine signals integrate reward and appetitive action in a temporally distinguishable, yet dependent, manner.

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Crossref · 10.1523/jneurosci.1527-22.2023

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  • The prospect of obtaining a reward such as a like or comment causes persistent dopamine release, encouraging the habit of monitoring social media regularly.

    “The prospect of obtaining a reward, such as a like or a comment, causes persistent dopamine release, encouraging the habit of monitoring social media regularly [12].”

    From The Impact of Social Media & Technology on Child and Adolescent Mental Health (2025) · cites this paper as [12]

    The Discussion reports sustained dopamine release in rats when a cue signaled an opportunity to act for a food reward, but not when it signaled reward delivery alone. The paper does not study likes, comments, social media, or habitual monitoring, so it does not support extending that finding to those behaviors. (LLM, conf=0.88)

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Authors
Goedhoop, J., Arbab, T., & Willuhn, I.
Affiliations
Netherlands Institute for Neuroscience (NL)
Corresponding author
Willuhn, Ingo
Venue
The Journal of Neuroscience
Published
2023-04-25
Volume
43
Issue
21
Pages
3922-3932
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W4366981293
Cited by
24
References
57
Citations by year
2026: 10 · 2025: 7 · 2024: 6 · 2023: 1
FWCI
2.91
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Pure Amsterdam UMC (publishedVersion, cc-by)
  • KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion, other-oa)
  • OSF Preprints (OSF Preprints) (submittedVersion)
Funders
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (024.004.012, 2015/06367/ALW, ERC-2014-STG 638013, 864.14.010)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
dopamine release, nucleus accumbens, mesolimbic dopamine system, reward prediction error, operant conditioning, classical conditioning, reward prediction, motivation, instrumental behavior
MeSH terms
Animals, Conditioning, Operant, Cues, Dopamine, Male, Motivation, Nucleus Accumbens, Reinforcement, Psychology, Reward, Rats, Sprague-Dawley, Rats

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