Conjunctive Processing of Locomotor Signals by the Ventral Tegmental Area Neuronal Population

Dong V Wang,Joe Z Tsien,Georges Chapouthier

doi:10.1371/journal.pone.0016528

Dong V Wang, Joe Z Tsien + Show 1 more

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https://doi.org/10.1371/journal.pone.0016528

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Abstract

The ventral tegmental area (VTA) plays an essential role in reward and motivation. How the dopamine (DA) and non-DA neurons in the VTA engage in motivation-based locomotor behaviors is not well understood. We recorded activity of putative DA and non-DA neurons simultaneously in the VTA of awake mice engaged in motivated voluntary movements such as wheel running. Our results revealed that VTA non-DA neurons exhibited significant rhythmic activity that was correlated with the animal's running rhythms. Activity of putative DA neurons also correlated with the movement behavior, but to a lesser degree. More importantly, putative DA neurons exhibited significant burst activation at both onset and offset of voluntary movements. These findings suggest that VTA DA and non-DA neurons conjunctively process locomotor-related motivational signals that are associated with movement initiation, maintenance and termination.

Highlights

The ventral tegmental area (VTA) is widely believed to play an essential role in reward, motivation and drug addiction [1,2,3,4,5]
Our results suggest that VTA putative DA and non-DA neurons conjunctively process locomotorrelated motivational signals that are associated with movement initiation, maintenance and termination
VTA putative DA neurons exhibit significant burst activation in response to the presentation of reward predicting cues, as well as at voluntary movement initiations and terminations. This general response property of the DA neuron is consistent with the notion that dopamine activity is more associated with motivation or ‘‘wanting’’ rather than hedonic impact of reward [3,10,11]

Summary

Introduction

The ventral tegmental area (VTA) is widely believed to play an essential role in reward, motivation and drug addiction [1,2,3,4,5]. Electrophysiological properties of putative dopamine (DA) neurons in the VTA have been extensively studied in previous studies, showing that unexpected reward (e.g., food, juice) and reward cues (conditioned stimuli) evoke a brief burst activity of the DA neurons [6,7,8,9]. These DA neurons’ responsiveness appears to encode a wide range of novel and reward-related events through a prediction error rule [6,7,8]. While non-DA neurons are presumed to play an important role in regulation of DA neurons in the VTA, few studies have examined their roles in animal’s motivational behaviors

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