Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine

Patricia A. Dombrowski, Tiago V. Maia, Suelen L. Boschen, Mariza Bortolanza, Etieli Wendler, Rainer K. W. Schwarting, Marcus Lira Brandao, Philip Winn, Charles D. Blaha, Claudio Da Cunha

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

We conducted an experiment in which hedonia, salience and prediction error hypotheses predicted different patterns of dopamine (DA) release in the striatum during learning of conditioned avoidance responses (CARs). The data strongly favor the latter hypothesis. It predicts that during learning of the 2-way active avoidance CAR task, positive prediction errors generated when rats do not receive an anticipated foot-shock (which is better than expected) cause DA release that reinforces the instrumental avoidance action. In vivo microdialysis in the rat striatum showed that extracellular DA concentration increased during early CAR learning and decreased throughout training returning to baseline once the response was well learned. In addition, avoidance learning was proportional to the degree of DA release. Critically, exposure of rats to the same stimuli but in an unpredictable, unavoidable, and inescapable manner, did not produce alterations from baseline DA levels as predicted by the prediction error but not hedonic or salience hypotheses. In addition, rats with a partial lesion of substantia nigra DA neurons, which did not show increased DA levels during learning, failed to learn this task. These data represent clear and unambiguous evidence that it was the factor positive prediction error, and not hedonia or salience, which caused increase in the tonic level of striatal DA and which reinforced learning of the instrumental avoidance response. (C) 2012 Published by Elsevier B.V.

LanguageEnglish
Pages112-119
Number of pages8
JournalBehavioural Brain Research
Volume241
DOIs
Publication statusPublished - 15 Mar 2013

Fingerprint

Corpus Striatum
Dopamine
Avoidance Learning
Learning
Operant Conditioning
Pleasure
Dopaminergic Neurons
Microdialysis
Substantia Nigra
Foot
Shock

Keywords

  • dopamine
  • prediction error
  • hedonia
  • salience
  • avoidance learning

Cite this

Dombrowski, P. A., Maia, T. V., Boschen, S. L., Bortolanza, M., Wendler, E., Schwarting, R. K. W., ... Da Cunha, C. (2013). Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine. Behavioural Brain Research, 241, 112-119. https://doi.org/10.1016/j.bbr.2012.06.031
Dombrowski, Patricia A. ; Maia, Tiago V. ; Boschen, Suelen L. ; Bortolanza, Mariza ; Wendler, Etieli ; Schwarting, Rainer K. W. ; Brandao, Marcus Lira ; Winn, Philip ; Blaha, Charles D. ; Da Cunha, Claudio. / Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine. In: Behavioural Brain Research. 2013 ; Vol. 241. pp. 112-119.
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Dombrowski, PA, Maia, TV, Boschen, SL, Bortolanza, M, Wendler, E, Schwarting, RKW, Brandao, ML, Winn, P, Blaha, CD & Da Cunha, C 2013, 'Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine' Behavioural Brain Research, vol. 241, pp. 112-119. https://doi.org/10.1016/j.bbr.2012.06.031

Evidence that conditioned avoidance responses are reinforced by positive prediction errors signaled by tonic striatal dopamine. / Dombrowski, Patricia A.; Maia, Tiago V.; Boschen, Suelen L.; Bortolanza, Mariza; Wendler, Etieli; Schwarting, Rainer K. W.; Brandao, Marcus Lira; Winn, Philip; Blaha, Charles D.; Da Cunha, Claudio.

In: Behavioural Brain Research, Vol. 241, 15.03.2013, p. 112-119.

Research output: Contribution to journalArticle

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AU - Maia, Tiago V.

AU - Boschen, Suelen L.

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AU - Wendler, Etieli

AU - Schwarting, Rainer K. W.

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