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

Abstract

Midbrain dopamine neurons are activated by reward or sensory stimuli predicting reward1–4. 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 while monkeys were conditioned using a Pavlovian procedure with appetitive and aversive outcomes (liquid reward and airpuff 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, more numerous dopamine neurons were excited by both of these stimuli, inconsistent with the hypothesis. Some dopamine neurons were also excited by both reward and airpuff 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 airpuff itself. These findings suggest that different groups of dopamine neurons convey motivational signals in distinct manners.

Where is the chocolate? Rapid spatial orienting toward stimuli associated with primary rewards

“…In this context, involuntary modulation of spatial attention orienting can be driven by two mechanisms: (a) initial orienting toward the emotional stimulus, or (b) difficulty in disengaging attention from the emotional stimulus and reallocating it toward another target (e.g., Posner, Inhoff, Friedrich, & Cohen, 1987). Research conducted in animals supports the hypothesis of initial orienting by showing an attentional bias generated by faster eye movements toward reward-associated stimuli (Matsumoto & Hikosaka, 2009). Recent studies showed similar results in humans, by demonstrating that reward associated stimuli were more likely to draw initial gaze than neutral stimuli (Anderson and Yantis, 2012a;Hickey & van Zoest, 2012;Theeuwes & Belopolsky, 2012), but the gaze is not maintained at that location for a longer period (Theeuwes & Belopolsky, 2012).…”

Computational models of reinforcement learning: the role of dopamine as a reward signal

“…The activity of some DA neurons in monkey SNc was also known to reflect the choice of the future motor response (Morris et al 2006). 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). Current computational models do not typically account for these data.…”

The role of learning-related dopamine signals in addiction vulnerability

“…In behavioral situations with contingencies changing about every 100 trials, dopamine neurons code the difference between current reward and reward history weighted by the last six to seven trials (Bayer et al, 2007). The occurrence of reward or reward prediction (positive prediction error) or their omission (negative prediction error) activates or depresses dopamine neurons in an inverse monotonic function of probability, such that the more unpredicted the event the stronger the response (de Lafuente and Romo, 2011;Enomoto et al, 2011;Fiorillo et al, 2003;Matsumoto and Hikosaka, 2009;Morris et al, 2006;Nakahara et al, 2004;Nomoto et al, 2010;Oyama et al, 2010;Satoh et al, 2003). Enomoto et al (2011) attempted to directly address whether the phasic dopamine response reflect the total future reward, as opposed to just the immediate reward.…”