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Two types of dopamine neuron distinctly convey positive and negative motivational signals

Nature volume 459, pages 837–841 (2009)Cite this article

Abstract

Midbrain dopamine neurons are activated by reward or sensory stimuli predicting reward1,2,3,4. These excitatory responses increase as the reward value increases5. This response property has led to a hypothesis that dopamine neurons encode value-related signals and are inhibited by aversive events. Here we show that this is true only for a subset of dopamine neurons. We recorded the activity of dopamine neurons in monkeys (Macaca mulatta) during a Pavlovian procedure with appetitive and aversive outcomes (liquid rewards and airpuffs directed at the face, respectively). We found that some dopamine neurons were excited by reward-predicting stimuli and inhibited by airpuff-predicting stimuli, as the value hypothesis predicts. However, a greater number of dopamine neurons were excited by both of these stimuli, inconsistent with the hypothesis. Some dopamine neurons were also excited by both rewards and airpuffs themselves, especially when they were unpredictable. Neurons excited by the airpuff-predicting stimuli were located more dorsolaterally in the substantia nigra pars compacta, whereas neurons inhibited by the stimuli were located more ventromedially, some in the ventral tegmental area. A similar anatomical difference was observed for their responses to actual airpuffs. These findings suggest that different groups of dopamine neurons convey motivational signals in distinct manners.

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Figure 1: Pavlovian procedure.
Figure 2: Responses of dopamine neurons to conditioned stimuli.
Figure 3: Responses of dopamine neurons to unconditioned stimuli.
Figure 4: Locations of dopamine neurons in relation to their responses to airpuff-predicting conditioned stimulus.

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Acknowledgements

We thank S. Hong, E. Bromberg-Martin, M. Yasuda, S. Yamamoto and Y. Tachibana for discussion, M. K. Smith for his histological expertise, J. W. McClurkin, A. M. Nichols, T. W. Ruffner, A. V. Hays and L. P. Jensen for technical assistance, and G. Tansey, D. Parker and B. Nagy for animal care. This research was supported by the Intramural Research Program at the National Institutes of Health, National Eye Institute.

Author Contributions M.M. designed the Pavlovian procedure, performed the experiments and analysed the data. O.H. supported all of these processes. M.M. and O.H. discussed the results and wrote the manuscript.

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Authors and Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435, USA ,

    Masayuki Matsumoto & Okihide Hikosaka

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  1. Masayuki Matsumoto
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  2. Okihide Hikosaka
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Correspondence to Masayuki Matsumoto.

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Matsumoto, M., Hikosaka, O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837–841 (2009). https://doi.org/10.1038/nature08028

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