Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors

• Published in: Nature neuroscience Vol. 19; no. 1; pp. 111 - 116
• Main Authors: Chang, Chun Yun, Esber, Guillem R, Marrero-Garcia, Yasmin, Yau, Hau-Jie, Bonci, Antonello, Schoenbaum, Geoffrey
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.01.2016; Nature Publishing Group
• Subjects: 631/378/116/2396; 631/378/1595/1395; Animal Genetics and Genomics; Animals; Anticipation, Psychological - physiology; Behavior, Animal - physiology; Behavioral Sciences; Biological Techniques; Biomedicine; Brain mapping; Brain research; Conditioning, Classical - physiology; Dopamine; Dopaminergic mechanisms; Dopaminergic Neurons - physiology; Electrophysiological Phenomena; Female; Genetic aspects; Health aspects; Hypotheses; Male; Neural circuitry; Neural Inhibition - physiology; Neurobiology; Neurons; Neurosciences; Optogenetics; Rats; Rats, Long-Evans; Rats, Transgenic; Reward; Reward (Psychology); Testing; Ventral Tegmental Area - physiology; New York; United States > US; Maryland; Baltimore Maryland
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/nn.4191

Phasic changes in dopamine activity correlate with prediction error signaling. But causal evidence that these brief changes in firing actually drive associative learning is rare. Here the authors show that brief pauses in dopamine neuron firing at the time of reward mimic the effects of endogenous negative prediction errors. Correlative studies have strongly linked phasic changes in dopamine activity with reward prediction error signaling. But causal evidence that these brief changes in firing actually serve as error signals to drive associative learning is more tenuous. Although there is direct evidence that brief increases can substitute for positive prediction errors, there is no comparable evidence that similarly brief pauses can substitute for negative prediction errors. In the absence of such evidence, the effect of increases in firing could reflect novelty or salience, variables also correlated with dopamine activity. Here we provide evidence in support of the proposed linkage, showing in a modified Pavlovian over-expectation task that brief pauses in the firing of dopamine neurons in rat ventral tegmental area at the time of reward are sufficient to mimic the effects of endogenous negative prediction errors. These results support the proposal that brief changes in the firing of dopamine neurons serve as full-fledged bidirectional prediction error signals.