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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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Lovic, V., Belay, H. T., Walker, C., Burton, C. L., Meaney, M. J., Sokolowski, M. B., & Fleming, A. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.09.046 · Cited by 33
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Appetitive behavioral traits and stimulus intensity influence maintenance of conditioned fear
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Sex and strain influence attribution of incentive salience to reward cues in mice
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Dopamine neurons drive spatiotemporally heterogeneous striatal dopamine signals during learning
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“Dopamine release in the nucleus accumbens (NAc) is critical for learning CS–US associations that result in sign-tracking (Dalley et al., 2002; Parkinson et al., 2002; Flagel et al., 2010), and while cue-evoked dopamine release in the NAc is reduced following extended training, Pavlovian approach behavior is still depe…”
BackgroundNoradrenergic contributions to cue-driven risk-taking and impulsivity
Chernoff, C. S., Hynes, T. J., & Winstanley, C. A. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05806-x · Cited by 32
Inferring spikes from calcium imaging in dopamine neurons
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Nigrostriatal dopamine signals sequence-specific action-outcome prediction errors
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Duration between rewards controls the rate of behavioral and dopaminergic learning
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“In line with prior work 5,35,39,40 , cue-evoked dopamine release developed over trials and preceded the emergence of cue-evoked licking (Fig.”
Cognitive and olfactory deficits in Machado–Joseph disease: A dopamine transporter study
Braga‐Neto, P., Felicio, A. C., Hoexter, M. Q., Pedroso, J. L., Dutra, L. A., Alessi, H., Minett, T., Santos, R. F., da Rocha, A. J., Garcia, L. Á. L., et al. (2012) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2012.04.015 · Cited by 29
Male rats that differ in novelty exploration demonstrate distinct patterns of sexual behavior.
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Self-citationRole of dopamine D2 receptors in optimizing choice strategy in a dynamic and uncertain environment
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“…behavior have not been elucidated, dopaminergic transmission in the NAc core is likely involved (Saddoris et al. 2016), as it has been shown to play a critical role in the sign-tracking but not the goal-tracking response (Flagel et al. 2011; Saunders and Robinson 2012; Yager et al. 2014).”
BackgroundInfluentialSelf-citationSchindler, A. G., Meabon, J. S., Pagulayan, K. F., Hendrickson, R. C., Meeker, K. D., Cline, M. M., Li, G., Sikkema, C. L., Wilkinson, C. W., Perl, D. P., et al. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.06.004 · Cited by 28
Self-citationThe Computational Complexity of Valuation and Motivational Forces in Decision-Making Processes
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A Role for Serotonin in Modulating Opposing Drive and Brake Circuits of Impulsivity
Desrochers, S. S., Spring, M. G., & Nautiyal, K. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.791749 · Cited by 29
“For example, the phenomenon of signtracking, where animals may interact with a manipulable cue as if it were the reward which it has come to be associated with, shows that a classically conditioned cue can acquire increased incentive salience (Flagel et al., 2011).”
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Paradoxical tolerance to cocaine after initial supersensitivity in drug‐use‐prone animals
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“…magnitude is associated with greater cue-induced DA release and greater appetitive responses (Beyene et al., 2010), it is possible that an enhanced pharmacological effect of cocaine in HR animals could lead to larger subsecond DA signals that underlie appetitive responding (Flagel et al., 2011).”
BackgroundPavlovian Conditioned Approach Training in Rats
Fitzpatrick, C. J., & Morrow, J. D. (2016) · Journal of Visualized Experiments · doi:10.3791/53580 · Cited by 29
A voxel-based analysis of neurobiological mechanisms in placebo analgesia in rats
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Disrupting reconsolidation: memory erasure or blunting of emotional/motivational value?
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“Finally, food and drug cues influence neural activity in brain regions that control motivated behavior to a greater extent in STs than in GTs [20–22, 30], and the acquisition and performance of ST, but not GT, is dopaminedependent [26, 38].”
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Distributional coding of associative learning in discrete populations of midbrain dopamine neurons
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“This explanation is also consistent with data demonstrating that rats given sensitizing doses of AMPH have higher levels of dopamine in NAc shell (Scholl, Feng, Watt, Renner, & Forster, 2009), as well as increased spine density and branching in the NAc (Robinson & Kolb, 1997).”
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“It will be interesting to extend these studies to quantification of neuroenergetic fluctuations that occur in response to more natural stimuli that activate the dorsal striatum, such as administration of psychostimulants [46], goal-directed behaviors [43, 44], or vigorous locomotion [45].”
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“There is a compelling argument that dopamine specifically encodes the state of incentive motivation, much of which comes from evidence that dopamine signaling is important for sign-tracking but not goal-tracking behavior (Berridge 2007; Flagel et al. 2011; Flagel and Robinson 2017).”
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Self-citationDoes reward unpredictability reflect risk?
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“…fast-scan cyclic voltammetry Dopamine (DA) has been implicated in various aspects of reward processing such as consumption (Wise, 1978, 1982), incentive value (Flagel et al, 2011), anticipation (Schultz, 1998) and the selection of appropriate action-outcome routines (Redgrave & Gurney, 2006).”
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Effects of nicotine self-administration on incentive salience in male Sprague Dawley rats
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Self-citationSign and goal tracker rats process differently the incentive salience of a conditioned stimulus
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“In addition, electrochemical studies have shown higher levels of dopamine release in nucleus accumbens (NAc) after CS presentation in ST animals [7].”
BackgroundSign tracking predicts suboptimal behavior in a rodent gambling task
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“2001; Flagel, 2011; Parkinson, 2002; Saunders and Robinson 2012).”
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Self-citationEarly life adversity potentiates expression of addiction-related traits
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Dopamine encodes deep network teaching signals for individual learning trajectories
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Role of ventral pallidal D2 dopamine receptors in the consolidation of spatial memory
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Dopamine Encodes Retrospective Temporal Information in a Context-Independent Manner
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“Moreover, the NAc is an important target of the mesolimbic dopamine (DA) projection, which carries information on reward-cue salience and reward prediction error [58, 59].”
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“In light of the demonstrated importance of dopamine in learning and memory processes (Di Chiara et al. 2004; Bassareo et al. 2011; Flagel et al. 2011), however, this more general posttrial impact of apomorphine is a strong possibility.”
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“Such a pattern bears some resemblance to the concept of behavioral impulsivity (Tomie et al., 1998; Flagel et al., 2010, 2011), and it is noteworthy in this context that the A1 allele has been linked to risk for impulsivity-related psychiatric disorders, most prominently alcohol dependence (Noble…”
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Past, Present, and Future of Tools for Dopamine Detection
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“It reproduces the difference in patterns of dopaminergic activity for GTs and STs (Flagel et al., 2011b).”
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Retrieval-Extinction and Relapse Prevention: Rewriting Maladaptive Drug Memories?
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“…cue-associated increases in DA in the NAc core of STs but not GTs, which underlie the attribution of incentive salience to reward-related cues (Flagel et al., 2011b), and administration of flupenthixol, a nonselective D1/D2 receptor antagonist, into the NAc core impairs the expression of…”
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Role of dopamine neurons in familiarity
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“There is compelling evidence that increased dopamine assigns salience to environmental stimuli (Berridge, 2007; Flagel et al., 2011; Kutlu et al., 2021).”
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“Crucially, relative to goal-trackers, signtrackers tend to present concomitant characteristics typically associated with compulsive reward-seeking behaviors such as addiction — namely, attentional deficits and personality traits such as novelty-seeking, riskseeking and impulsivity [39,41,13].”
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“Our findings are similar to the recent finding with oICSS that the mesolimbic DA was closely associated with Pavlovian conditioning or cue-conditioned secondary reward [28, 41, 42].”
ResultMolas, S., Zhao-Shea, R., Freels, T. G., & Tapper, A. R. (2023) · eNeuro · doi:10.1523/eneuro.0282-22.2022 · Cited by 26
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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