Two types of dopamine neuron distinctly convey positive and negative motivational signals.
Midbrain dopamine neurons are activated by reward or sensory stimuli predicting reward. These excitatory responses increase as the reward value increases. 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.
Matsumoto
Masayuki
M
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435, USA. matsumotom@nei.nih.gov
Hikosaka
Okihide
O
D000388:Air; D000818:Animals; D001070:Appetitive Behavior / Q000502:physiology; D003214:Conditioning, Classical / Q000502:physiology; D004298:Dopamine / Q000378:metabolism*; D008253:Macaca mulatta / Q000502:physiology*; D008959:Models, Neurological; D009042:Motivation; D009474:Neurons / Q000502:physiology*; D012201:Reward
D004298:Dopamine