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A selective role for dopamine in stimulus-reward learning
Open accessAbstract
Individuals make choices and prioritize goals using complex processes that assign value to rewards and associated stimuli. During Pavlovian learning, previously neutral stimuli that predict rewards can acquire motivational properties, becoming attractive and desirable incentive stimuli. However, whether a cue acts solely as a predictor of reward, or also serves as an incentive stimulus, differs between individuals. Thus, individuals vary in the degree to which cues bias choice and potentially promote maladaptive behaviour. Here we use rats that differ in the incentive motivational properties they attribute to food cues to probe the role of the neurotransmitter dopamine in stimulus–reward learning. We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors. Rather, dopamine acts selectively in a form of stimulus–reward learning in which incentive salience is assigned to reward cues. In individuals with a propensity for this form of learning, reward cues come to powerfully motivate and control behaviour. This work provides insight into the neurobiology of a form of stimulus–reward learning that confers increased susceptibility to disorders of impulse control.
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TL;DR
Dopamine is not required for all forms of stimulus-reward learning; it selectively supports the attribution of incentive salience to reward cues. In rats, sign-trackers show increasing CS-evoked and decreasing US-evoked nucleus accumbens dopamine during Pavlovian conditioning, and dopamine antagonism prevents acquisition of sign-tracking but not goal-tracking conditioned responses.
Key findings
- Systemic flupenthixol attenuated performance of the conditioned response in both bHRs and bLRs, but only bHRs failed to acquire a sign-tracking CR when trained on drug; on drug-free session 8, bHRs still failed to show sign-tracking (P≤0.01 vs saline), whereas bLRs showed a fully developed goal-tracking CR (session 8 vs session 1, P≤0.0002; vs bLR saline, P≥0.6).
- During acquisition, CS-evoked dopamine release increased in bHRs relative to unpaired controls (pairing × session: F(5,35)=4.58, P=0.003) but not bLRs (F(5,35)=0.94, P=0.46); trial-by-trial correlation with trial number was significant for bHR (r²=0.14, P<0.0001) but not bLR (r²=0.003, P=0.54), with different slopes (P=0.005) and higher CS-evoked dopamine in bHRs after acquisition (session six, P=0.04).
- US-evoked dopamine release was lower after acquisition in bHRs (session six, P=0.002), and CS and US signals diverged in bHRs (stimulus × session: F(5,40)=5.47, P=0.0006) but not bLRs (F(5,40)=0.28, P=0.92).
- Outbred rats reproduced the pattern: sign-trackers showed increased CS-evoked and decreased US-evoked dopamine during learning (stimulus × session: F(5,50)=4.43, P=0.002), whereas goal-trackers did not (F(5,40)=0.48, P=0.72); the lever-CS was also a more effective conditioned reinforcer in bHRs than bLRs (phenotype × group interaction for active nose pokes: F(1,33)=4.82, P=0.04).
Methods
- Adult male Sprague-Dawley rats from a selective-breeding colony (bHR/bLR, generations S18–S22) and commercially obtained outbred rats underwent Pavlovian conditioning with a lever-CS paired with food; conditioned responses were classified as sign-tracking (approach lever-CS) or goal-tracking (approach food-tray).
- Fast-scan cyclic voltammetry at carbon-fiber microelectrodes in the nucleus accumbens core measured phasic dopamine (scans every 100 ms, 10 Hz) during conditioning; recording sites were verified histologically.
- Flupenthixol (i.p.) was given for performance (150, 300, or 600 μg/kg before sessions 9, 11, 13, counterbalanced with saline before sessions 8, 10, 12, 14) and for acquisition (225 μg/kg before sessions 1–7); main analyses used ANOVA/ANOVA with session as a continuous variable and correlations.
Limitations
- Stated: the neural mechanisms underlying sign-tracking and goal-tracking behavior remain to be elucidated; the neurochemical data alone do not rule out the possibility that prediction-error signals are present in other dopamine terminal regions.
- Stated: the post-acquisition flupenthixol finding needs cautious interpretation because of a non-specific effect on activity.
- Evident from the text: the causal dopamine manipulation was systemic flupenthixol, and the sample was male rats (selectively bred plus outbred); no female or human data are reported.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Systemic administration of flupenthixol, a nonspecific dopamine receptor antagonist, attenuated performance of the CR for both bHRs and bLRs.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“With training, bHRs came to rapidly approach and engage the lever-CS (Fig. 1a-b)”
§ A selective role for dopamine in reward learning > Abstract
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This effect was clearly evident when the antagonist was administered during training (Fig. 4, sessions 1–7).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“First, US-evoked dopamine release in the nucleus accumbens decreased during training in sign-trackers, but not in goal-trackers.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIn the paper
“Moreover, in outbred rats where this baseline difference in responding does not exist, we have found similar results, indicating that the lever-CS is a more effective conditioned reinforcer for sign-trackers than goal-trackers13.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [13] Boakes, R. in Operant-Pavlovian Interactions (eds Davis, H. & Hurwitz, H. M. B.) 67–97 (Erlbaum, 1977)
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Importantly, experiments conducted in commercially-obtained outbred rats reproduced the pattern of dopamine release observed in the selectively-bred rats (Fig. 3, Fig. S4).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We show that intact dopamine transmission is not required for all forms of learning in which reward cues become effective predictors.”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: It has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Importantly, rats that received non-contiguous (pseudorandom) presentations of the CS and the US did not learn either a sign-tracking or a goal-tracking CR (Fig. 1e).”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“During four additional sessions, the profound differences in dopamine release between sign- and goal-trackers were stable (Fig. S5), demonstrating that these differences are not limited to the initial stages of learning.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“whereas upon CS presentation bLRs came to rapidly approach and engage the location where food would be delivered (Fig. 1c-d; see detailed statistics in Supplementary Information).”
§ A selective role for dopamine in reward learning > Abstract
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passes
- It may state two separate claims as one. 33
- The quote only partly states this claim. 1
- Probably not a substantial claim. 4
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Both bHRs and bLRs acquired their respective CRs as a function of training, as there was a significant effect of session for all measures of sign-tracking behavior for bHRs (a-b; P≤0.0001), and of goal-tracking behavior for bLRs (c-d; P≤0.0001).”
§ A selective role for dopamine in reward learning > Abstract
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“US-evoked dopamine release also differed between bHR and bLR rats during training (session x phenotype interaction: F(5,40) = 6.09, P = 0.0003), but for this stimulus dopamine release was lower after acquisition in bHRs (session six; P = 0.002; Fig. S4).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Indeed, the trial-by-trial correlation between CS-evoked dopamine release and trial number was significant for bHR (r2=0.14, P < 0.0001) but not bLR (r2=0.003, P=0.54) rats, producing significantly different slopes (P=0.005) and higher CS-evoked dopamine release in bHR rats after acquisition (Fig. S4, session six; P = 0.04).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“During the acquisition of conditioned approach, CS-evoked dopamine release (Fig. 2, Fig. S3) increased in bHR rats relative to unpaired controls (pairing x session interaction: F(5,35) = 4.58, P = 0.003), but there was no such effect in bLRs (Fig. 2, Fig. S3; pairing x session interaction: F(5,35) = 0.94, P = 0.46).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“Third, bHR rats that underwent Pavlovian training in the presence of a dopamine receptor antagonist did not acquire a sign-tracking CR, consistent with previous reports24; however, dopamine antagonism had no effect on learning a goal-tracking CR in bLR rats.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [24] Clark, J. J. et al. Chronic microsensors for longitudinal, subsecond dopamine detection in behaving animals. Nature Methods 7, 126–129 (2010) source
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Furthermore, bHRs and bLRs learned their respective CRs at the same rate, as indicated by analyses of variance in which session was treated as a continuous variable and the phenotypes were directly compared.”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one. The quote only partly states this claim.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The CS and US signals diverge in bHR rats (stimulus x session interaction: F(5,40) = 5.47, P = 0.0006; Fig. 2c) but not bLR rats (stimulus x session interaction: F(5,40) = 0.28, P = 0.92; Fig. 2f).”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Specifically, there was an increase in CS-evoked and a decrease in US-evoked dopamine release during learning in outbred rats that learned a sign-tracking CR (stimulus x session interaction: F(5,50) = 4.43, P = 0.002; Fig. 3d), but not in those that learned a goal-tracking CR (stimulus x session interaction: F(5,40) = 0.48, P = 0.72; Fig. 3f).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“When presentation of a lever-CS was paired with food delivery both bHRs and bLRs developed a Pavlovian CR, but as we have described previously15, the topography of the CR was different in the two groups.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [15] Stead, J. D. et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36, 697–712 (2006) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the lever-CS was a more effective conditioned reinforcer in bHR than bLR animals, as indicated by a significant phenotype x group interaction for active nose pokes (F(1,33)=4.82, P=0.04), which controls for “basal” differences in nosepoke responding.”
§ A selective role for dopamine in reward learning > Abstract
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast, flupenthixol had no effect on learning the CS-US association that lead to a goal-tracking CR (P≥0.6 vs. saline, session 8; Fig. 4d-f), because on the drug-free session bLRs showed a fully developed goal-tracking CR—their session 8 performance differed significantly from their session 1 performance (P≤0.0002).”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Both conditioned bHRs and bLRs made more active than inactive nose pokes, and more active nose pokes than control groups that received pseudorandom presentations of the CS and the US (Fig. 1f-g; detailed statistics in Supplementary Information).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Second, the CS evoked dopamine release in both sign- and goal-tracking rats, but this signal increased to a greater degree in sign-trackers, which attributed incentive salience to the CS.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Similar to surgically naïve animals, bHRs learned a sign-tracking CR (session effect on lever contacts: F(5,20) = 5.76, P = 0.002) and bLRs a goal-tracking CR (session effect on food-receptacle contacts: F(5,20) = 5.18, P = 0.003) during neurochemical data collection (Fig. S2).”
§ A selective role for dopamine in reward learning > Abstract
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“It was also observed after the rats had already acquired their respective CR (Fig. S6), but this latter finding needs to be interpreted cautiously because of a non-specific effect on activity (Figure S6e).”
§ A selective role for dopamine in reward learning > Abstract
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
In the paper
“Outbred rats with similar baseline locomotor activity13 and similar baseline levels of reward-related dopamine release in the nucleus accumbens (see Fig. 3), differ in whether they are prone to learn a sign-tracking or goal-tracking CR, but they still develop patterns of dopamine release specific to that CR.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [13] Boakes, R. in Operant-Pavlovian Interactions (eds Davis, H. & Hurwitz, H. M. B.) 67–97 (Erlbaum, 1977)
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, learning a goal-tracking CR does not require intact dopamine transmission, whereas learning a sign-tracking CR does.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: It has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In summary, the lever-CS was equally predictive, evoking a CR in both groups, but it acquired two properties of an incentive stimulus to a greater degree in bHRs than bLRs: it was more attractive, as indicated by approach behavior (Fig. 1a) and more desirable, as indicated by the ability to serve as a conditioned reinforcer (Fig. 1f).”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Phasic neurotransmission in the mesolimbic dopamine system is initially triggered by the receipt of reward (unconditional stimulus; US), but shifts to a cue predictive of reward (conditional stimulus; CS) after associative learning3,4.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [3] Day, J. J., Roitman, M. F., Wightman, R. M. & Carelli, R. M. Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nature Neurosci. 10, 1020–1028 (2007) source
- Not checked yetcites [4] Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“However, only in sign-trackers is the CS an attractive incentive stimulus, and only in sign-trackers is it strongly desired (i.e. “wanted”), in the sense that animals will work avidly to get it13.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [13] Boakes, R. in Operant-Pavlovian Interactions (eds Davis, H. & Hurwitz, H. M. B.) 67–97 (Erlbaum, 1977)
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“These behavioral phenotypes are accompanied by baseline differences in dopamine transmission, with bHRs showing elevated sensitivity to dopamine agonists, increased proportion of striatal D2receptors in a high-affinity state, greater frequency of spontaneous dopamine transients15, and higher reward-related dopamine release prior to conditioning, all of which could enhance their attribution of in”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [15] Stead, J. D. et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36, 697–712 (2006) source
- Not checked yetcites [29] Wyvell, C. L. & Berridge, K. C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J. Neurosci. 20, 8122–8130 (2000) source
- Not checked yetcites [30] Wyvell, C. L. & Berridge, K. C. Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J. Neurosci. 21, 7831–7840 (2001) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, while dopamine may be necessary for the performance of both sign-tracking and goal-tracking CRs, it is only necessary for acquisition of a sign-tracking CR, indicating that these forms of learning are mediated by distinct neural systems.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“The selectively-bred rats used in this study have distinctive behavioral phenotypes, including greater behavioral disinhibition and reduced impulse control in bHRs15.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [15] Stead, J. D. et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36, 697–712 (2006) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“More importantly, when examined off flupenthixol during the 8th test session, bHRs still failed to demonstrate a sign-tracking CR (P≤0.01 vs. saline, session 8; Fig. 4a-c), indicating that dopamine is necessary for both the performance and the learning of a sign-tracking CR, consistent with previous findings20.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [20] Dalley, J. W. et al. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl Acad. Sci. USA 102, 6189–6194 (2005) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“The core of the nucleus accumbens is an important anatomical substrate for motivated behavior17,18 and has been specifically implicated as a site where dopamine acts to mediate the acquisition and/or performance of Pavlovian conditioned approach behavior19–22.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [17] Berridge, K. C. in Psychology of Learning and Motivation (ed. Medin, D. L.) 223–278 (Academic Press, 2001)
- Not checked yetcites [18] Cardinal, R. N., Parkinson, J. A., Hall, J. & Everitt, B. J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352 (2002) source
- Not checked yetcites [19] Kelley, A. E. Functional specificity of ventral striatal compartments in appetitive behaviors. Ann. NY Acad. Sci. 877, 71–90 (1999) source
- Not checked yetcites [20] Dalley, J. W. et al. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl Acad. Sci. USA 102, 6189–6194 (2005) source
- Not checked yetcites [21] Di Ciano, P., Cardinal, R. N., Cowell, R. A., Little, S. J. & Everitt, B. J. Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J. Neurosci. 21, 9471–9477 (2001) source
- Not checked yetcites [22] Parkinson, J. A. et al. Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav. Brain Res. 137, 149–163 (2002) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“In rats selectively-bred for differences in locomotor responses to a novel environment14, high responders to novelty (bHR) consistently learn a sign-tracking CR but low responders to novelty (bLR) consistently learn a goal-tracking CR15.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [14] Robinson, T. E. & Flagel, S. B. Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol. Psychiat. 65, 869–873 (2009) source
- Not checked yetcites [15] Stead, J. D. et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36, 697–712 (2006) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The CS is an effective predictor in animals that learn either a sign-tracking or a goal-tracking response; it acts as an “excitor”, evoking a CR in both.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Another feature of an incentive stimulus is to be “wanted” and as such animals should work to obtain it10,16.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [10] Berridge, K. C., Robinson, T. E. & Aldridge, J. W. Dissecting components of reward: 'liking', 'wanting', and learning. Curr. Opin. Pharmacol. 9, 65–73 (2009) source
- Not checked yetcites [16] Flagel, S. B. et al. An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology 35, 388–400 (2010) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Collectively, these data provide several lines of evidence demonstrating that dopamine does not act as a universal teaching signal in reward learning, but selectively participates in a form of stimulus-reward learning whereby Pavlovian incentive value is attributed to a CS.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: It has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.
In the paper
“Human motivated behavior is subject to a wide span of individual differences ranging from highly deliberative to highly impulsive actions directed towards the acquisition of rewards32.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [32] Kuo, W. J., Sjostrom, T., Chen, Y. P., Wang, Y. H. & Huang, C. Y. Intuition and deliberation: two systems for strategizing in the brain. Science 324, 519–522 (2009) source
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The current work demonstrates that dopamine-encoded prediction-error signals are indeed present in the nucleus accumbens of sign-trackers, but not in the accumbens of goal-trackers.”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:boosted· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In sum, we show that dopamine is an integral part of reward learning that is specifically associated with the attribution of incentive salience to reward cues.”
§ A selective role for dopamine in reward learning > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: It has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.
None of the sources cited for this claim have been checked yet.
In the paper
“Previous research using site-specific dopamine antagonism20 and dopamine-specific lesions21 indicated that dopamine acts in the nucleus accumbens core to support the learning and performance of sign-tracking behavior.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [20] Dalley, J. W. et al. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl Acad. Sci. USA 102, 6189–6194 (2005) source
- Not checked yetcites [21] Di Ciano, P., Cardinal, R. N., Cowell, R. A., Little, S. J. & Everitt, B. J. Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J. Neurosci. 21, 9471–9477 (2001) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Although these neurochemical data alone do not rule out the possibility that prediction-error signals are present in other dopamine terminal regions, the results from systemic dopamine antagonism demonstrate that intact dopamine transmission is generally not required for learning of a goal-tracking CR.”
§ A selective role for dopamine in reward learning > Abstract
Load-bearingStrength:boosted· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Individuals who attribute reward cues with incentive salience find it more difficult to resist such cues, a feature associated with reduced impulse control15,31.”
§ A selective role for dopamine in reward learning > Abstract
What the sources say
- Not checked yetcites [15] Stead, J. D. et al. Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet. 36, 697–712 (2006) source
- Not checked yetcites [31] Tomie, A., Aguado, A. S., Pohorecky, L. A. & Benjamin, D. Ethanol induces impulsive-like responding in a delay-of-reward operant choice procedure: impulsivity predicts autoshaping. Psychopharmacology 139, 376–382 (1998) source
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
The paper relies on this without support.
It has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.
“To date, it has been difficult to determine whether dopamine mediates the predictive or the motivational properties of reward-associated cues, because these two features are often acquired together.”
The paper relies on this without support.
The neural mechanisms underlying sign-tracking and goal-tracking behavior remain to be elucidated.
“The neural mechanisms underlying sign-tracking and goal-tracking behavior remain to be elucidated.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“These attentional influences are difficult to overcome and may underlie maladaptive reactions in psychiatric disorders, such as the enhanced susceptibility of addicted patients to drug-related cues (Flagel et al., 2011).”
From Attention, learning, and the value of information (2012) · cites this paper as Flagel et al., 2011
In the citing paper
“Although not guided by reliability or expected information, this form of attention is a powerful mechanism, which automatically draws resources to stimuli that have intrinsic emotional or conditioned associations (Damaraju et al., 2009; Flagel et al., 2011; Hickey et al., 2010a, b; Hogarth et al., 2010; Libera and Chelazzi, 2009; Vuilleumier, 2005).”
From Attention, learning, and the value of information (2012) · cites this paper as Flagel et al., 2011
Statistics that don’t add up
Each reported p-value recomputed from its test statistic and degrees of freedom.
Inconsistent p-value: F(5,40) = 0.48, p = .72
MinorThe paper reports p = .72 here; recomputing from the test statistic and its degrees of freedom gives p = .789. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p = .72 · recomputed p = .789
“F(5,40) = 0.48, P = 0.72”
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Doesn’t add upF(5, 40) = 0.48reported p = .72 · recomputed p = .789
“F(5,40) = 0.48, p = .72”
- ConsistentF(1, 236) = 3.02reported p = .08 · recomputed p = .084
“F(1,236)=3.02, p = .08”
- ConsistentF(1, 236) = 0.93reported p = .34 · recomputed p = .336
“F(1,236)=0.93, p = .34”
- ConsistentF(1, 33) = 4.82reported p = .04 · recomputed p = .035
“F(1,33)=4.82, p = .04”
- ConsistentF(5, 20) = 5.76reported p = .002 · recomputed p = .002
“F(5,20) = 5.76, p = .002”
- ConsistentF(5, 20) = 5.18reported p = .003 · recomputed p = .003
“F(5,20) = 5.18, p = .003”
- ConsistentF(5, 40) = 10.5reported p < .0001 · recomputed p < .001
“F(5,40) = 10.5, p < .0001”
- ConsistentF(1, 8) = 0.13reported p = .73 · recomputed p = .728
“F(1,8) = 0.13, p = .73”
- ConsistentF(5, 40) = 1.16reported p = .35 · recomputed p = .346
“F(5,40) = 1.16, p = .35”
- ConsistentF(5, 35) = 4.58reported p = .003 · recomputed p = .003
“F(5,35) = 4.58, p = .003”
- ConsistentF(5, 35) = 0.94reported p = .46 · recomputed p = .467
“F(5,35) = 0.94, p = .46”
- ConsistentF(5, 40) = 6.09reported p = .0003 · recomputed p < .001
“F(5,40) = 6.09, p = .0003”
- ConsistentF(5, 40) = 5.47reported p = .0006 · recomputed p < .001
“F(5,40) = 5.47, p = .0006”
- ConsistentF(5, 40) = 0.28reported p = .92 · recomputed p = .921
“F(5,40) = 0.28, p = .92”
- ConsistentF(5, 50) = 4.43reported p = .002 · recomputed p = .002
“F(5,50) = 4.43, p = .002”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Self-check results appear here once an independent check has confirmed them.
Citations
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Cortes, P. M., Hernández‐Arteaga, E., Sotelo-Tapia, C., Guevara, M. Á., Medina, A. C., & González, M. H. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112593 · Cited by 11
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Fast-Scan Voltammetry for In Vivo Measurements of Neurochemical Dynamics
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Preclinical Studies Shed Light on Individual Variation in Addiction Vulnerability
Saunders, B. T., Yager, L. M., & Robinson, T. E. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.161 · Cited by 11
Self-citationSelf-administration of agonists selective for dopamine D2, D3, and D4 receptors by rhesus monkeys
Koffarnus, M. N., Collins, G. T., Rice, K. C., Chen, J., Woods, J. H., & Winger, G. D. (2012) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3283564dbb · Cited by 11
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“…such as the attribution of incentive salience or behavioral reactivity (Salamone, 1988, 1992, 1994, Peciña Berridge and Parker 1997, Garris et al. 1999, Cannon and Palmiter 2003, Phillips et al. 2003, Cannon and Bseikri 2004, Roitman et al. 2004, Robinson et al. 2005, Flagel et al. 2011).”
BackgroundMorphine Reward Promotes Cue-Sensitive Learning: Implication of Dorsal Striatal CREB Activity
Baudonnat, M., Guillou, J., Husson, M., Bohbot, V. D., Schwabe, L., & David, V. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00087 · Cited by 12
Guaita, G. D. O., Vecchia, D. D., Andreatini, R., Robinson, D. L., Schwarting, R. K. W., & Cunha, C. D. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4878-8 · Cited by 11
Translation of Computational Psychiatry in the Context of Addiction
Liu, S., Dolan, R. J., & Heinz, A. (2020) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2020.1637 · Cited by 11
Nicotine Enhances Goal-Tracking in Ethanol and Food Pavlovian Conditioned Approach Paradigms
Angelyn, H., Loney, G. C., & Meyer, P. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.561766 · Cited by 12
Howe, W., Tierney, P. L., Young, D., Oomen, C., & Kozak, R. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3955-5 · Cited by 10
The role of the nucleus accumbens in learned approach behavior diminishes with training
Dobrovitsky, V., West, M. O., & Horvitz, J. C. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14523 · Cited by 10
“Other work, separating sign tracking from goal tracking, shows that while DA receptor blockade disrupts the expression of both (Flagel et al., 2011), NAc and NAc DA play particularly important roles in sign tracking (Flagel et al.”
BackgroundDinu, L. M., Georgescu, A. L., Singh, S. N., Byrom, N., Overton, P. G., Singer, B. F., & Dommett, E. J. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.114846 · Cited by 13
Current perspectives on brain circuits involved in food addiction-like behaviors
Senol, E., & Mohammad, H. (2024) · Journal of Neural Transmission · doi:10.1007/s00702-023-02732-4 · Cited by 11
“Dopamine is released on the medium spiny neurons (MSN) within the NAc expressing dopamine receptors (D1R and D2R) in the striatum, implicated in regulating motivated behaviors (Flagel et al. 2011; Kauer and Malenka 2007; Salamone and Correa 2012).”
Schettino, M., Tarmati, V., Castellano, P., Gigli, V., Carnevali, L., Cabib, S., Ottaviani, C., & Orsini, C. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100647 · Cited by 10
“…conditioned approach behavior and reinforcement learning requires dopamine transmission in the core region of the NAc, rather than in the NAcSh (Flagel et al., 2011; Aitken et al., 2016; Grima et al., 2022), while habit learning (the other subconstruct of reward learning) engages the…”
InfluentialCross-kingdom regulation of gene expression in giant pandas via plant-derived miRNA
Tan, H., Wang, C., Feng, L., Peng, Y., Sima, J., Li, Y., Deng, L., Wu, K., Xu, Z., & Zhang, Z. (2025) · Frontiers in Veterinary Science · doi:10.3389/fvets.2025.1509698 · Cited by 12
“Recent studies have highlighted the critical role of dopamine in stimulus reward learning behavior (48).”
Intersection of effort and risk: ethological and neurobiological perspectives
Miller, M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00208 · Cited by 11
Persistent coding of outcome-predictive cue features in the rat nucleus accumbens
Gmaz, J. M., Carmichael, J. E., & van der Meer, M. A. A. (2018) · eLife · doi:10.7554/elife.37275 · Cited by 15
Kypriotakis, G., Cinciripini, P. M., & Versace, F. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108753 · Cited by 11
Tabbara, R. I., Maddux, J.-M. N., Beharry, P. F., Iannuzzi, J., & Chaudhri, N. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000138 · Cited by 10
A general framework for innovative mobile biofeedback based educational games
Forstner, B., Szegletes, L., Angeli, R., et al. (2013) · IEEE International Conference on Cognitive Infocommunications · doi:10.1109/coginfocom.2013.6719204 · Cited by 10
The Functions of Dopamine in Operant Conditioned Reflexes
Maiorov, V. I. (2019) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-019-00815-y · Cited by 10
Effects of inter-trial interval on sign-tracking and conditioned reinforcer efficacy in female rats
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Pavlovian-instrumental interactions in active avoidance: The bark of neutral trials
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Cinotti, F., Marchand, A. R., Roesch, M. R., Girard, B., & Khamassi, M. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05323-y · Cited by 10
“Note that in the original STGT model aimed at accounting for the experimental results of Flagel and colleagues (Flagel et al. 2011), there were no pure MB agents, but simulated goal-trackers had a very small parameter ω < 0.05, which means that the FMF system was contributing to less than 5% of…”
InfluentialJordan, R., & Keller, G. B. (2023) · eLife · doi:10.7554/elife.85111.2 · Cited by 9
Servonnet, A., Rompré, P.-P., & Samaha, A. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114254 · Cited by 9
Prediction error in dopamine neurons during associative learning
Amo, R. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.07.003 · Cited by 11
“2A) (Clark et al., 2013; Day et al., 2007; Flagel et al., 2011; Hollerman and Schultz, 1998; Menegas et al., 2017; Pan et al., 2005), there had been no experimental observation reported for the "gradual" temporal shift of dopamine activation from reward timing to cue onset (Fig.”
BackgroundEye understand: Physiological measures as novel predictors of adaptive learning in horses
Evans, L., Cameron‐Whytock, H. A., & Ijichi, C. L. (2023) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2023.106152 · Cited by 9
Proietti, R., Parr, T., Tessari, A., Friston, K. J., & Pezzulo, G. (2025) · Physics of Life Reviews · doi:10.1016/j.plrev.2025.05.008 · Cited by 17
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Gyawali, U., Martin, D. A., Sun, F., Li, Y., & Calu, D. J. (2023) · eLife · doi:10.7554/elife.81980 · Cited by 9
Dundon, C. M., & Rellini, A. H. (2012) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2012.02799.x · Cited by 8
Why don’t guiding cues always guide in behavior chains?
Reid, A. K., Rapport, H. F., & Le, T.-A. P. (2013) · Learning & Behavior · doi:10.3758/s13420-013-0115-9 · Cited by 9
Nonkes, L. J. P., van de Vondervoort, I. I. G. M., & Homberg, J. R. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.11.017 · Cited by 9
Fitzpatrick, C. J., Perrine, S. A., Ghoddoussi, F., Galloway, M. P., & Morrow, J. D. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13524 · Cited by 9
“Although it is known that dopaminergic transmission within the NAc core is critical for the expression of sign-tracking behavior (Flagel et al. 2011b; Saunders andRobinson 2012;Yager et al. 2014), the relationship of other neurochemicals in the NAc, mPFC, and HPC to sign-tracking behavior is poorly…”
BackgroundMelis, M. R., Sanna, F., & Argiolas, A. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0058 · Cited by 9
“…to dopaminergic drugs (e.g. psychostimulants) but lower D2 mRNA and D2 receptor binding compared to NELR rats (Hooks et al., 1991, 1994; Flagel et al., 2010; Garcia-Fuster et al., 2010), and that bNEHR rats are more prone to self-administer cocaine (Davis et al., 2008; Cummings…”
BackgroundPreproenkephalin-expressing ventral pallidal neurons control inhibitory avoidance learning
Macpherson, T., Mizoguchi, H., Yamanaka, A., & Hikida, T. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.02.011 · Cited by 9
“Interestingly, these two conditioned responses have been demonstrated to be controlled by distinct neural mechanisms, with activity in dopamine release in the NAc and NAc D1-neuron activation necessary for sign-tracking but not goal-tracking behavior (Flagel et al., 2011; Macpherson and Hikida, 2018).”
Mode of Sucrose Delivery Alters Reward-Related Phasic Dopamine Signals in Nucleus Accumbens
McCutcheon, J. E., & Roitman, M. F. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00262 · Cited by 9
Network of evolvable neural units can learn synaptic learning rules and spiking dynamics
Bertens, P., & Lee, S. (2020) · Nature Machine Intelligence · doi:10.1038/s42256-020-00267-x · Cited by 16
Conditioned approach behavior of SHR and SD rats during Pavlovian conditioning
Silic, B., Aggarwal, M., Liyanagama, K., Tripp, G., & Wickens, J. R. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114348 · Cited by 10
“increased response to reward delivery has been associated with goal tracking behavior [73].”
Freedberg, M., Schacherer, J., Chen, K., Uc, E. Y., Narayanan, N. S., & Hazeltine, E. (2017) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-017-0505-0 · Cited by 11
Werlen, E., Shin, S.-L., Gastambide, F., François, J., Tricklebank, M. D., Marston, H. M., Huxter, J. R., Gilmour, G., & Walton, M. E. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0564-8 · Cited by 10
“It has been demonstrated that dopamine release in the core region of the NAc correlates with a RPE, and similar to that observed here, dynamically changes over the course of learning [9, 10, 14, 50, 51] (see ref.”
The incentive salience of the stimuli biases rats’ preferences in the “suboptimal choice” procedure
Orduña, V., & Alba, R. (2020) · Behavioural Processes · doi:10.1016/j.beproc.2020.104057 · Cited by 8
Schettino, M., Mauti, M., Parrillo, C., Ceccarelli, I., Giove, F., Napolitano, A., Ottaviani, C., Martelli, M., & Orsini, C. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-03162-w · Cited by 12
“Dopaminergic signaling within the ventral striatum, speci fi cally within the core of the Nucleus Accumbens (NAc), is critical for the development and expression of ST behavior [3, 6, 7], aligning with dopamine ’ s role in attributing incentive salience [8].”
BackgroundResultUsing rodent data to elucidate dopaminergic mechanisms of ADHD: Implications for human personality
Tripp, G., & Wickens, J. R. (2024) · Personality Neuroscience · doi:10.1017/pen.2023.12 · Cited by 9
“…cues and higher phasic dopamine response to reward delivery display more goal-tracking behavior, and conversely, animals with a higher striatal dopamine response to reward-predicting cues and lower dopamine response to reward delivery display more sign-tracking behavior (Flagel et al., 2012).”
BackgroundSu, H., Ye, T., Cao, S., & Hu, C. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1416222 · Cited by 13
“This proposition was further confirmed by systemic administration of flupenthixol, a non-selective dopamine antagonist, which showed that blocking dopamine had an impact on learning in the ST system within the PCA, while the GT system remained largely unaffected (Flagel et al., 2010).”
BackgroundResultDopamine builds and reveals reward-associated latent behavioral attractors
Naudé, J., Sarazin, M., Mondoloni, S., Hannesse, B., Vicq, É., Amegandjin, F., Mourot, A., Fauré, P., & Delord, B. (2024) · Nature Communications · doi:10.1038/s41467-024-53976-x · Cited by 11
“Indeed, cues paired withreward induce both the releaseof DA and an increase in motor responses 31 , confounding the interpretation of the role of DA in subsequent behavior.”
Recommender systems use in weight management mHealth interventions: A scoping review
Castro, B. A., Levens, S. M., Sullivan, M., & Shaw, G. (2024) · Obesity Reviews · doi:10.1111/obr.13863 · Cited by 11
The incentive amplifying effects of nicotine: Roles in alcohol seeking and consumption
King, C. P., & Meyer, P. (2022) · Advances in pharmacology · doi:10.1016/bs.apha.2021.10.008 · Cited by 10
Afshar, N. M., Cinotti, F., Martin, D. A., Khamassi, M., Calu, D. J., Taylor, J. R., & Groman, S. M. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1113-22.2022 · Cited by 7
Cocker, P. J., Haar, C. V., & Winstanley, C. A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.007 · Cited by 8
Vicario-Feliciano, R. M., Murray, E. A., & Averbeck, B. B. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000211 · Cited by 9
Sign- and goal-tracking rats show differences in various executive functions
Enkel, T., Bartsch, D., & Bähner, F. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111979 · Cited by 7
Analysis of memory modulation by conditioned stimuliPreprint
Lapointe, T., Wolter, M., & Leri, F. (2021) · Learning & Memory · doi:10.1101/lm.052407.120 · Cited by 7
Cofresí, R. U., Upton, S., Brown, A. A., Piasecki, T. M., Bartholow, B. D., & Froeliger, B. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100156 · Cited by 6
Machine Learning for Neurotransmitter Monitoring by Fast Voltammetry: Current and Future Prospects
Movassaghi, C. S., & Andrews, A. M. (2025) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5c00543 · Cited by 7
Modularity of mind and the role of incentive motivation in representing novelty
Anselme, P. (2012) · Animal Cognition · doi:10.1007/s10071-012-0499-5 · Cited by 7
“In contrast, rats exposed to the 100 % probability expressed more goaltracking behaviour, that is, they went to the food magazine while the lever was still illuminated, suggesting that their behaviour was more cognitively than motivationally driven (Flagel et al. 2011).”
BackgroundReframing dopamine: A controlled controller at the limbic-motor interface
Lloyd, K., & Dayan, P. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011569 · Cited by 8
The regional specificity of rapid actions of cocaine
Aragona, B. J. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3043-c1 · Cited by 5
Elaboration of a model of Pavlovian learning and performance: HeiDI.
Honey, R. C., Dwyer, D. M., & Iliescu, A. F. (2020) · Journal of Experimental Psychology Animal Learning and Cognition · doi:10.1037/xan0000239 · Cited by 7
“…with the lever, others by investigating the location where the reinforcer is about to be delivered, with the remaining rats showing patterns of behavior in between these two extremes (e.g., Iliescu et al., 2018; Flagel et al., 2009, 2011; Patitucci et al., 2016; see also, Matzel et al., 2003).”
Reinstatement of Pavlovian responses to alcohol cues by stress
Armstrong, A., Rosenthal, H. B., Stout, N., & Richard, J. M. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06255-w · Cited by 6
Pawlowsch-Instrumentelle Transfereffekte bei Alkoholabhängigkeit
Genauck, A., Huys, Q. J. M., Heinz, A., & Rapp, M. A. (2013) · SUCHT - Zeitschrift für Wissenschaft und Praxis / Journal of Addiction Research and Practice · doi:10.1024/0939-5911.a000256 · Cited by 7
Lomanowska, A. M., & Kraemer, G. W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.062 · Cited by 8
Munro, M. F. (2015) · Nature · doi:10.1038/522s46a · Cited by 7
Incidental learning of rewarded associations bolsters learning on an associative task.
Freedberg, M., Schacherer, J., & Hazeltine, E. (2015) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/xlm0000201 · Cited by 7
Spanos, M., Xie, X., Gras-Najjar, J., White, S. H., & Sombers, L. A. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00492 · Cited by 9
Colorimetric Sensing of Dopamine Based on Peroxidase-Like Activity of Gold Nanoparticles
Jiang, C., Pang, S., Luo, J., et al. (2019) · Journal of Analytical Chemistry · doi:10.1134/s1061934819070049 · Cited by 7
Jupp, B., Jones, J. A., & Dalley, J. W. (2019) · Handbook of experimental pharmacology · doi:10.1007/164_2019_300 · Cited by 6
Lopez, S. A., Mubarak, E., Yang, C., Parsegian, A., Klumpner, M. S., Campus, P., & Flagel, S. B. (2021) · eNeuro · doi:10.1523/eneuro.0384-20.2021 · Cited by 7
Self-citationEvaluation of miRNA as Biomarkers of Emotional Valence in Pigs
Marsh, L., Hutchinson, M. R., McLaughlan, C. J., Musolino, S. T., Hebart, M. L., Terry, R., Verma, P. J., Hiendleder, S., & Whittaker, A. L. (2021) · Animals · doi:10.3390/ani11072054 · Cited by 8
“Given that DA is implicated in behavioural control and is essential for reward related processes including reward learning [54,55], we anticipated this same difference to be reflected in the judgment bias data.”
ResultA Network State Linking Motivation and Action in the Nucleus Accumbens
Catanese, J., & van der Meer, M. A. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.021 · Cited by 7
“For instance, Flagel et al. (2011) demonstrated that in a related (Pavlovian) procedure—using a light cue, rather than a sound, paired with reward availability— rats either approach the cue (‘‘sign 754 Neuron 78, June 5, 2013 ª2013 Elsevier tracking’’) or the reward site itself (‘‘goal tracking’’),…”
BackgroundYan, T., Rizak, J. D., Wang, J., et al. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00273 · Cited by 7
Esumi, S., Kawasaki, Y., Nakamoto, A., Sagara, H., Gomita, Y., Kitamura, Y., & Sendo, T. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.09.079 · Cited by 8
Probing the Neurochemical Correlates of Motivation and Decision Making
Wassum, K. M., & Phillips, P. E. M. (2014) · ACS Chemical Neuroscience · doi:10.1021/cn500322y · Cited by 8
Self-citationJordan, R., & Keller, G. B. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.08.515698 · Cited by 7
Bender, B. N., Stringfield, S. J., & Torregrossa, M. M. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100149 · Cited by 6
Peart, D. R., Nolan, C. J., Stone, A. P., Williams, M. A., Karlovcec, J. M., & Murray, J. E. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06584-y · Cited by 7
“This conditioned induction of dopamine release is required for expression of goal tracking in simple conditioning tasks (Flagel et al. 2011; Wassum et al. 2011).”
Distinct cholinergic circuits underlie discrete effects of reward on attention
Runyon, K., Bui, T., Mazanek, S., Hartle, A. E., Marschalko, K., & Howe, W. M. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1429316 · Cited by 8
“But why?” Dopamine and causal learning
Namboodiri, V. M. K. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101443 · Cited by 6
How dopamine guides our social world
Padilla-Coreano, N., & Martínez-Rivera, F. J. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100085 · Cited by 6
Recruitment of specific dopamine neuron sub-circuits by opioids
Morison, S. L., Doster, L. B., Vigotsky, A. D., Centeno, M. V., del Rey, N. L., Apkarian, A. V., & Awatramani, R. B. (2025) · Addiction Neuroscience · doi:10.1016/j.addicn.2025.100233 · Cited by 8
Unveiling Dopamine and Met-Enkephalin Dynamics: Simultaneous Co-Detection in Rat Striatum
Berger, J. M., Todorov, J., Turner, K. M., McCarty, G. S., Romanova, E. V., Sweedler, J. V., & Sombers, L. A. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.5c03599 · Cited by 6
Ford, G., Bhakta, B., Cozens, A., Cundill, B., Hartley, S., Holloway, I., Meads, D., Pearn, J., Ruddock, S., Sackley, C., et al. (2019) · Efficacy and Mechanism Evaluation · doi:10.3310/eme06050 · Cited by 6
Gibney, K. D., Kypriotakis, G., & Versace, F. (2023) · Addiction Neuroscience · doi:10.1016/j.addicn.2023.100106 · Cited by 10
Derman, R. C., Bryda, E. C., & Ferrario, C. R. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114768 · Cited by 6
“This seems unlikely given that NAc dopamine in response to CS presentation remains high during extinction training in sign-trackers [16,17].”
InfluentialRethinking dopamine‐guided action sequence learning
Song, M. R., & Lee, S. W. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16426 · Cited by 6
“…invigora-tion (Berke, 2018; Blesa et al., 2022; Da Silva et al., 2018; Howe & Dombeck, 2016; Klaus et al., 2019; Syed et al., 2015) and incentive learning (Berridge, 2007; Flagel et al., 2011; Fraser, Pribut, et al., 2023; Saunders et al., 2018; Wise, 2004), is involved in all of these processes.”
BackgroundEffects of the cannabinoid receptor agonist CP-55,940 on incentive salience attribution
Gheidi, A., Cope, L. M., Fitzpatrick, C. J., Froehlich, B., Atkinson, R., Groves, C. K., Barcelo, C. N., & Morrow, J. D. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05571-3 · Cited by 5
The Role of Intra-Amygdaloid Neurotensin and Dopamine Interaction in Spatial Learning and Memory
László, B. R., Kertes, E., Ollmann, T., Péczely, L., Kovács, A., Karádi, Z., Lénárd, L., & László, K. (2022) · Biomedicines · doi:10.3390/biomedicines10123138 · Cited by 6
Neuro-Immune Modulation of Cholinergic Signaling in an Addiction Vulnerability Trait
Carmon, H., Haley, E. C., Parikh, V., Tronson, N. C., & Sarter, M. F. (2023) · eNeuro · doi:10.1523/eneuro.0023-23.2023 · Cited by 5
Townsend, E. S., Amaya, K. A., Smedley, E. B., & Smith, K. S. (2023) · Scientific Reports · doi:10.1038/s41598-023-40439-4 · Cited by 8
“ACh receptors can modulate dopamine (DA) signaling 27,29–33 , including cue-evoked DA release that is required for the maintenance and acquisition of the sign-tracking response 23 .”
BackgroundNeuronal and psychological underpinnings of pathological gambling
Singer, B. F., Anselme, P., Robinson, M. J. F., & Vezina, P. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00230 · Cited by 8
Sullivan, L. J., Shaffer, H., Hill, C., & Arco, A. D. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.111972 · Cited by 6
Maiolati, M., Tarmati, V., Latagliata, E. C., Cabib, S., & Orsini, C. (2021) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000629 · Cited by 6
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McKendrick, G., Sharma, S., Sun, D., Randall, P. A., & Graziane, N. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173638 · Cited by 6
Evolution of in vivo dopamine monitoring techniques
Yocky, A. G., & Covey, D. P. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173078 · Cited by 8
Finan, P. H., Letzen, J. E., Epstein, D. H., Mun, C. J., Stull, S. W., Kowalczyk, W. J., Agage, D. A., Phillips, K. A., Pizzagalli, D. A., & Preston, K. L. (2021) · Pain Medicine · doi:10.1093/pm/pnab031 · Cited by 6
“Dopamine is an essential substrate of reward responsiveness [6], supporting cognitive and motivational states that fuel the pursuit of a wide array of natural rewards [7–11].”
Background
Metadata
- Authors
- Flagel, S. B., Clark, J. J., Robinson, T. E., Mayo, L., Czuj, A., Willuhn, I., Akers, C. A., Clinton, S. M., Phillips, P. E. M., & Akil, H.
- Affiliations
- University of Michigan (US)
- University of Washington (US)
- Corresponding author
- Phillips, Paul E. M.
- Akil, Huda
- ORCID
- Venue
- Nature
- Published
- 2010-12-08
- Volume
- 469
- Issue
- 7328
- Pages
- 53-57
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3058375
- OpenAlex
- W2116049552
- Semantic Scholar
- 38476c39379a177d3b95fa22125a1a7f09116670
- Cited by
- 1,026
- References
- 41
- Citations by year
- 2026: 43 · 2025: 45 · 2024: 56 · 2023: 54 · 2022: 63 · 2021: 57 · 2020: 101 · 2019: 60 · 2018: 55 · 2017: 58 · 2016: 84 · 2015: 82 · 2014: 80 · 2013: 85 · 2012: 59
- FWCI
- 24.20
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (2t32da007278-31)
- National Institute of Mental Health (R00MH085859, R01MH079292)
- National Institute on Drug Abuse (F32-DA24540, P01DA021633, T32-DA07278, T32-DA007278, F32DA024540, R37DA004294, R37 DA04294, R01DA027858)
- 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, incentive salience, classical conditioning, incentive motivation, food cues, selective breeding, dopamine receptor blockade, cyclic voltammetry, individual differences, impulse control disorders, drug addiction
- MeSH terms
- Animals, Conditioning, Classical, Cues, Dopamine, Flupenthixol, Food, Disruptive, Impulse Control, and Conduct Disorders, Learning, Male, Microelectrodes, Models, Neurological, Motivation, Synaptic Transmission, Nucleus Accumbens, Phenotype, Probability, Reward, Signal Transduction, Rats, Sprague-Dawley, Dopamine Antagonists, Rats
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