Phasic dopamine release induced by positive feedback predicts individual differences in reversal learning.
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.
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands; Department of Psychiatry, Academic Medical Center, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands. Electronic address: m.klanker@nin.knaw.nl.
Marianne
M
Klanker
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands.
Tessa
T
Sandberg
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands.
Ruud
R
Joosten
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands; Department of Psychiatry, Academic Medical Center, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands.
Ingo
I
Willuhn
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands; Department of Psychiatry, Academic Medical Center, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands.
Matthijs
M
Feenstra
Netherlands Institute for Neuroscience, Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, The Netherlands; Department of Psychiatry, Academic Medical Center, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands.
Damiaan
D
Denys
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D003216:Conditioning, Operant / Q000502:physiology*; D003342:Corpus Striatum / Q000378:metabolism*; D003463:Cues; D004193:Discrimination Learning / Q000502:physiology; D004298:Dopamine / Q000378:metabolism*; D007206:Individuality; D008297:Male; D051381:Rats; D012193:Reversal Learning / Q000502:physiology*; D012201:Reward
D004298:Dopamine
Cognitive flexibility; Dopamine; Fast-scan cyclic voltammetry; Feedback learning; Reversal learning