Phasic dopamine release induced by positive feedback predicts individual differences in reversal learning

TY - JOUR

T1 - Phasic dopamine release induced by positive feedback predicts individual differences in reversal learning

AU - Klanker, Marianne

AU - Sandberg, Tessa

AU - Joosten, R.N.J.M.A.

AU - Willuhn, Ingo

AU - Feenstra, M.G.P.

AU - Denys, D.

N1 - Copyright © 2015 Elsevier Inc. All rights reserved.

PY - 2015/11

Y1 - 2015/11

N2 - Striatal dopamine (DA) is central to reward-based learning. Less is known about the contribution of DA to the ability to adapt previously learned behavior in response to changes in the environment, such as a reversal of response-reward contingencies. We hypothesized that DA is involved in the rapid updating of response-reward information essential for successful reversal learning. We trained rats to discriminate between two levers, where lever availability was signaled by a non-discriminative cue. Pressing one lever was always rewarded, whereas the other lever was never rewarded. After reaching stable discrimination performance, a reversal was presented, so that the previously non-rewarded lever was now rewarded and vice versa. We used fast-scan cyclic voltammetry to monitor DA release in the ventromedial striatum. During discrimination performance (pre-reversal), cue presentation induced phasic DA release, whereas reward delivery did not. The opposite pattern was observed post-reversal: Striatal DA release emerged after reward delivery, while cue-induced release diminished. Trial-by-trial analysis showed rapid reinstatement of cue-induced DA release on trials immediately following initial correct responses. This effect of positive feedback was observed in animals that learned the reversal, but not in 'non-learners'. In contrast, neither pre-reversal responding and DA signaling, nor post-reversal DA signaling in response to negative feedback differed between learners and non-learners. Together, we show that phasic DA dynamics in the ventromedial striatum encoding reward-predicting cues are associated with positive feedback during reversal learning. Furthermore, these signals predict individual differences in learning that are not present prior to reversal, suggesting a distinct role for dopamine in the adaptation of previously learned behavior.

AB - Striatal dopamine (DA) is central to reward-based learning. Less is known about the contribution of DA to the ability to adapt previously learned behavior in response to changes in the environment, such as a reversal of response-reward contingencies. We hypothesized that DA is involved in the rapid updating of response-reward information essential for successful reversal learning. We trained rats to discriminate between two levers, where lever availability was signaled by a non-discriminative cue. Pressing one lever was always rewarded, whereas the other lever was never rewarded. After reaching stable discrimination performance, a reversal was presented, so that the previously non-rewarded lever was now rewarded and vice versa. We used fast-scan cyclic voltammetry to monitor DA release in the ventromedial striatum. During discrimination performance (pre-reversal), cue presentation induced phasic DA release, whereas reward delivery did not. The opposite pattern was observed post-reversal: Striatal DA release emerged after reward delivery, while cue-induced release diminished. Trial-by-trial analysis showed rapid reinstatement of cue-induced DA release on trials immediately following initial correct responses. This effect of positive feedback was observed in animals that learned the reversal, but not in 'non-learners'. In contrast, neither pre-reversal responding and DA signaling, nor post-reversal DA signaling in response to negative feedback differed between learners and non-learners. Together, we show that phasic DA dynamics in the ventromedial striatum encoding reward-predicting cues are associated with positive feedback during reversal learning. Furthermore, these signals predict individual differences in learning that are not present prior to reversal, suggesting a distinct role for dopamine in the adaptation of previously learned behavior.

U2 - 10.1016/j.nlm.2015.08.011

DO - 10.1016/j.nlm.2015.08.011

M3 - Article

C2 - 26343836

VL - 125

SP - 135

EP - 145

JO - Neurobiology of Learning and Memory

JF - Neurobiology of Learning and Memory

SN - 1074-7427

ER -