TY - JOUR
T1 - Anticipation of Appetitive Operant Action Induces Sustained Dopamine Release in the Nucleus Accumbens
AU - Goedhoop, Jessica
AU - Arbab, Tara
AU - Willuhn, Ingo
N1 - Funding Information: Received Aug. 9, 2022; revised Feb. 28, 2023; accepted Mar. 7, 2023. Author contributions: J.G. and I.W. designed research; J.G. performed research; J.G. and I.W. analyzed data; and J.G., T.A., and I.W. wrote the paper. This research was supported by European Research Council Grant ERC-2014-STG 638013 and Netherlands Organization for Scientific Research Grants 2015/06367 and BRAINSCAPES 024.004.012. We thank Ralph Hamelink and Nicole Yee for technical support. The authors declare no competing financial interests. Correspondence should be addressed to Ingo Willuhn at ingo.willuhn@gmail.com. https://doi.org/10.1523/JNEUROSCI.1527-22.2023 Copyright © 2023 Goedhoop et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Publisher Copyright: Copyright © 2023 Goedhoop et al.
PY - 2023/5/24
Y1 - 2023/5/24
N2 - 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: male 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 5 s cue presentation (preceding the required action). This dopamine ramp was unaffected by probabilistic reward delivery, occurred exclusively before operant actions, and was not related to task performance or task acquisition as it persisted throughout the 2 week daily behavioral training. Instead, the ramp flexibly increased in duration with longer cue presentation, seemingly modulating the initial cue-onset-triggered dopamine release, that is, the reward prediction error (RPE) signal, as both signal amplitude and sustainment 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.
AB - 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: male 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 5 s cue presentation (preceding the required action). This dopamine ramp was unaffected by probabilistic reward delivery, occurred exclusively before operant actions, and was not related to task performance or task acquisition as it persisted throughout the 2 week daily behavioral training. Instead, the ramp flexibly increased in duration with longer cue presentation, seemingly modulating the initial cue-onset-triggered dopamine release, that is, the reward prediction error (RPE) signal, as both signal amplitude and sustainment 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.
KW - dopamine
KW - motivated behavior
KW - nucleus accumbens
KW - operant conditioning
KW - pavlovian conditioning
KW - striatum
UR - http://www.scopus.com/inward/record.url?scp=85160205364&partnerID=8YFLogxK
U2 - https://doi.org/10.1523/JNEUROSCI.1527-22.2023
DO - https://doi.org/10.1523/JNEUROSCI.1527-22.2023
M3 - Article
C2 - 37185100
SN - 0270-6474
VL - 43
SP - 3922
EP - 3932
JO - Journal of neuroscience
JF - Journal of neuroscience
IS - 21
ER -