How do dopamine neurons represent positive and negative motivational events?

By Masayuki Matsumoto, Okihide Hikosaka. Nature, 2009

1,295 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/b484ad105a5651f12e97635f615d02cea425ba2f

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Citations in the corpus

Dopamine neurons encoding long-term memory of object value for habitual behavior (2015, neutral): “Recent studies suggest that DA neurons are heterogeneous in terms of their functions (Brischoux et al., 2009; Lerner et al., 2015; Matsumoto and Hikosaka, 2009).”
Whole-brain mapping of direct inputs to midbrain dopamine neurons. (2012, positive): “Indeed, a recent study in nonhuman primates found at least two types of dopamine neurons, saliency coding and value coding, that are activated and inhibited, respectively, by aversive events (Matsumoto and Hikosaka, 2009).”
Neuron-type specific signals for reward and punishment in the ventral tegmental area (2012, methodology): “Conventionally, spike waveforms and other firing properties have been used to identify presumed dopaminergic and GABAergic neuron”
Updating dopamine reward signals (2013, background): “Would salience explain the higher incidence of responses to conditioned aversive stimuli (35–65%) compared to unpredicted air puffs (<15%) [34,37]? The physical salience of small conditioned visual stimuli is marginal [34,36,37] and higher with air puffs and electric shocks.”
Circuit Architecture of VTA Dopamine Neurons Revealed by Systematic Input–Output Mapping (2015, background): “Although most DA neurons were activated by reward and reward-predictive cues, some were activated by noxious or salient stimuli (Brischoux et al., 2009; Matsumoto and Hikosaka, 2009; Zweifel et al., 2011).”
Model-Based and Model-Free Pavlovian Reward Learning: Revaluation, Revision and Revelation (2014, background): “Some complications do arise from the spatial heterogeneity for valence coding that has particularly been observed in the VTA (but see Matsumoto & Hikosaka, 2009), with one group of dopamine neurons being excited by unexpected punishments (rather than being suppressed, as might naively be expected…”
Dopaminergic reward system: a short integrative review (2010, background): “It has been demonstrated that a progressive loss of neuromelanin-containing DA neurons in the SNc of the ventral midbrain inducing DA depletion in the striatum, and it has been suggested that this deficit induces motor symptoms associated with PD, including bradykinesia, tremor, rigidity and loss of”
Computational models of reinforcement learning: the role of dopamine as a reward signal (2010, background): “In addition, the activity of a population of DA neurons in the monkey SNc was shown to increase in response to stimuli predicting punishments (Matsumoto and Hikosaka 2009).”
Neuronal Reward and Decision Signals: From Theories to Data. (2015, background): “Salience, rather than negative reinforcer value, might also explain the surprising higher incidence of activations to conditioned stimuli compared with primary punishment (345).”
The feedback-related negativity (FRN) revisited: New insights into the localization, meaning and network organization (2014, background): “…our findings are in linewith the recently stated theory that dopaminergic neurons also encode |RPE|-like salience signals (Bromberg-Martin et al., 2010a, 2010b; Matsumoto and Hikosaka, 2009) which are most probably also projected to the anterior cingulate cortex (Bromberg-Martin et al., 2010b).”