Motor skill learning and reward consumption differentially affect VTA activation

Susan Leemburg,Andreas Luft,Tara Canonica

doi:10.1038/s41598-017-18716-w

Susan Leemburg, Andreas Luft + Show 1 more

Open Access

https://doi.org/10.1038/s41598-017-18716-w

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Abstract

Dopamine release from the ventral tegmental area (VTA) terminals in the primary motor cortex (M1) enables motor skill acquisition. Here, we test the hypothesis that dopaminergic VTA neurons projecting to M1 are activated when rewards are obtained during motor skill acquisition, but not during task execution at plateau performance, or by rewards obtained without performing skilled movements. Rats were trained to perform a skilled reaching task for 3 days (acquisition) or 7 days (plateau). In combination with retrograde labelling of VTA-to-M1 projection neurons, double immunofluorescence for c-fos and tyrosine hydroxylase (TH) was used to assess activation of dopaminergic and non-dopaminergic VTA neurons. Dopaminergic VTA-to-M1 projection neurons were indeed activated during successful motor skill acquisition, but not when rats failed to learn or had reached plateau performance, nor by food rewards alone. By contrast, dopaminergic VTA neurons that did not project to M1 were activated by both skilled reaching and food rewards. Non-dopaminergic neurons were found to be activated by motor task performance at plateau, but not during skill acquisition. These results indicate that distinct populations of VTA neurons are activated by motor skill acquisition and task performance. Moreover, this activation is not merely related to consumption of food rewards.

Highlights

Dopamine release from the ventral tegmental area (VTA) to the nucleus accumbens and the frontal cortex plays an important role in reward processing and supports a variety of reinforcement learning processes[1,2]
Most of the tracer was found within M1 and had not spread to subcortical areas, a small amount of FastBlue was present in secondary motor cortex directly adjacent to M1 (Fig. 1C)
C-fos expression in VTA neurons is low at baseline, increased c-fos expression VTA neurons has been described in a variety of learning tasks, including classical conditioning, simple operant conditioning tasks, as well as conditioning to drugs of abuse[20,21,22,23,24]

Summary

Introduction

Dopamine release from the ventral tegmental area (VTA) to the nucleus accumbens and the frontal cortex plays an important role in reward processing and supports a variety of reinforcement learning processes[1,2]. Inhibition of VTA activity prevents task acquisition[1,3,5,6], suggesting an essential role for VTA dopamine release in a variety of learning tasks. But not execution of an already learned skill, depends on dopamine release from VTA projections to the primary motor cortex (M1)[7,8]. We test the hypothesis that activation of VTA-to-M1 dopaminergic neurons is induced by motor skill acquisition, but not by task performance at plateau after learning has ended, or by reward consumption that does not require skilled movements. Each experiment included a matched control group of rats that received a food reward at the same time as the paired skilled reaching rat, as well as an untrained, unrewarded control group

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