Abstract
Dopamine neurons are thought to encode novelty in addition to reward prediction error (the discrepancy between actual and predicted values). In this study, we compared dopamine activity across the striatum using fiber fluorometry in mice. During classical conditioning, we observed opposite dynamics in dopamine axon signals in the ventral striatum ('VS dopamine') and the posterior tail of the striatum ('TS dopamine'). TS dopamine showed strong excitation to novel cues, whereas VS dopamine showed no responses to novel cues until they had been paired with a reward. TS dopamine cue responses decreased over time, depending on what the cue predicted. Additionally, TS dopamine showed excitation to several types of stimuli including rewarding, aversive, and neutral stimuli whereas VS dopamine showed excitation only to reward or reward-predicting cues. Together, these results demonstrate that dopamine novelty signals are localized in TS along with general salience signals, while VS dopamine reliably encodes reward prediction error.
Highlights
Animals respond to new stimuli in a characteristic way across species, historically characterized as an ‘orienting reflex’ or a ‘what is it reflex’ (Pavlov and Anrep, 1927; Sechenov, 1935; Sokolov, 1963)
The results demonstrate that new odors activate dopamine neurons projecting to the tail of the striatum, but that this activity fades as the novelty wears off
ventral striatum (VS) dopamine gradually developed responses to reward-predicting cues during learning. These findings revealed that dopamine novelty coding is localized to the posterior part of the striatum, while VS dopamine faithfully encodes reward prediction error
Summary
Animals respond to new stimuli in a characteristic way across species, historically characterized as an ‘orienting reflex’ or a ‘what is it reflex’ (Pavlov and Anrep, 1927; Sechenov, 1935; Sokolov, 1963). Detection of novel stimuli is advantageous for survival because novel stimuli can signal potential rewards or potential threats. Orienting towards a novel stimulus and understanding it through exploration can allow future exploitation of potential rewards. In addition to behavioral advantages, novelty detection is fundamental for computation in our brain. Novelty detectors, or ‘novelty filters’ (Kohonen and Oja, 1976; Marsland et al, 2002), can reduce the amount of total information so that we can focus on unexpected perceptions as inputs to pay attention to and to learn from. Behavioral studies have repeatedly shown that both humans and other animals have enhanced memory for novel items (Kishiyama et al, 2009; Restorff, 1933)
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