Abstract

Dopamine neurons in the ventral tegmental area (VTA) have been traditionally studied for their roles in reward-related motivation or drug addiction. Here we study how the VTA dopamine neuron population may process fearful and negative experiences as well as reward information in freely behaving mice. Using multi-tetrode recording, we find that up to 89% of the putative dopamine neurons in the VTA exhibit significant activation in response to the conditioned tone that predict food reward, while the same dopamine neuron population also respond to the fearful experiences such as free fall and shake events. The majority of these VTA putative dopamine neurons exhibit suppression and offset-rebound excitation, whereas ∼25% of the recorded putative dopamine neurons show excitation by the fearful events. Importantly, VTA putative dopamine neurons exhibit parametric encoding properties: their firing change durations are proportional to the fearful event durations. In addition, we demonstrate that the contextual information is crucial for these neurons to respectively elicit positive or negative motivational responses by the same conditioned tone. Taken together, our findings suggest that VTA dopamine neurons may employ the convergent encoding strategy for processing both positive and negative experiences, intimately integrating with cues and environmental context.

Highlights

  • Dopamine neurons in the ventral tegmental area (VTA) have been traditionally studied for their roles in reward-related motivation or drug addiction [1,2,3]

  • Data from 24 mice from which we recorded putative dopamine neurons were used in the current analyses

  • We found that VTA dopamine neurons exhibited diverse response properties and the vast majority of the putative dopamine neurons respond to both reward and fearful stimuli

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Summary

Introduction

Dopamine neurons in the ventral tegmental area (VTA) have been traditionally studied for their roles in reward-related motivation or drug addiction [1,2,3]. The role of the dopamine neuron in positive motivation has been well established and supported by many studies showing that reward (e.g., food, juice) and reward cues (conditioned stimuli) evoke a short-latency (50–110 ms) and shortduration (,200 ms) burst activity of the dopamine neuron [5,6,7,8,9]. Dopamine levels can exhibit opposite functions in reinforcement on behavior: the lower dopamine level in the nucleus accumbens is believed to improve punishment- but impairs reward-based learning, while the higher dopamine level improves reward- but impairs punishment-based learning [18] These above studies strongly suggest that VTA dopamine neurons play an important role in processing negative motivational signals. The exact role of the VTA dopamine neuron in negative motivation is not fully clear

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