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The Journal of Neuroscience, November 5, 2008, 28(45):11673-11684; doi:10.1523/JNEUROSCI.3839-08.2008

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Behavioral/Systems/Cognitive
Midbrain Dopaminergic Neurons and Striatal Cholinergic Interneurons Encode the Difference between Reward and Aversive Events at Different Epochs of Probabilistic Classical Conditioning Trials

Mati Joshua,^1,2 Avital Adler,^1,2 Rea Mitelman,^1,2 Eilon Vaadia,^1,2 and Hagai Bergman^1,2,3

¹Department of Physiology, The Hebrew University–Hadassah Medical School, Jerusalem 91120, Israel, and ²The Interdisciplinary Center for Neural Computation and ³Eric Roland Center for Neurodegenerative Diseases, The Hebrew University, Jerusalem 91904, Israel

Correspondence should be addressed to Mati Joshua, Department of Physiology, The Hebrew University–Hadassah Medical School, P.O. Box 12272, Jerusalem 91120, Israel. Email: mati{at}alice.nc.huji.ac.il

Midbrain dopaminergic neurons (DANs) typically increase their discharge rate in response to appetitive predictive cues and outcomes, whereas striatal cholinergic tonically active interneurons (TANs) decrease their rate. This may indicate that the activity of TANs and DANs is negatively correlated and that TANs can broaden the basal ganglia reinforcement teaching signal, for instance by encoding worse than predicted events. We studied the activity of 106 DANs and 180 TANs of two monkeys recorded during the performance of a classical conditioning task with cues predicting the probability of food, neutral, and air puff outcomes. DANs responded to all cues with elevations of discharge rate, whereas TANs depressed their discharge rate. Nevertheless, although dopaminergic responses to appetitive cues were larger than their responses to neutral or aversive cues, the TAN responses were more similar. Both TANs and DANs responded faster to an air puff than to a food outcome; however, DANs responded with a discharge elevation, whereas the TAN responses included major negative and positive deflections. Finally, food versus air puff omission was better encoded by TANs. In terms of the activity of single neurons with distinct responses to the different behavioral events, both DANs and TANs were more strongly modulated by reward than by aversive related events and better reflected the probability of reward than aversive outcome. Thus, TANs and DANs encode the task episodes differentially. The DANs encode mainly the cue and outcome delivery, whereas the TANs mainly encode outcome delivery and omission at termination of the behavioral trial episode.

Key words: primate; basal ganglia; spike train; reinforcement; substantia nigra; striatum

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Received Aug. 13, 2008; accepted Sept. 16, 2008.

Correspondence should be addressed to Mati Joshua, Department of Physiology, The Hebrew University–Hadassah Medical School, P.O. Box 12272, Jerusalem 91120, Israel. Email: mati{at}alice.nc.huji.ac.il

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