Motor skill learning and reward consumption differentially affect VTA activation

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.