Midbrain dopamine and striatal tonically active neurons (TANs, presumed acetylcholine interneurons) signal behavioral significance of environmental events. Since striatal dopamine and acetylcholine affect plasticity of cortico-striatal transmission and are both crucial to learning, they may serve as teachers in the basal ganglia circuits. We recorded from both neuronal populations in monkeys performing a probabilistic instrumental conditioning task. Both neuronal types respond robustly to reward-related events. Although different events yielded responses with different latencies, the responses of the two populations coincided, indicating integration at the target level. Yet, while the dopamine neurons' response reflects mismatch between expectation and outcome in the positive domain, the TANs are invariant to reward predictability. Finally, TAN pairs are synchronized, compared to a minority of dopamine neuron pairs. We conclude that the striatal cholinergic and dopaminergic systems carry distinct messages by different means, which can be integrated differently to shape the basal ganglia responses to reward-related events.
Bibliographical noteFunding Information:
We thank S. Haber, Y. Ben-Shaul, and Y. Prut for fruitful discussions and comments on earlier versions of this manuscript; W. Schultz and C. Fiorillo for sharing their method of recording DA neurons; G. Goelman for MRI; and V. Sharkansky for technical assistance. This study was partly supported by a center of excellence grant administered by the ISF, by the United States-Israel Binational Science Foundation, by the German-Israel Binational Foundation (GIF), and by the BMBF Israel-Germany collaboration in medical research. G.M. was supported by the Horowitz fellowship.