Motor skill learning and reward consumption differentially affect VTA activation.

Susan Leemburg, Tara Canonica, Andreas Luft
Author Information
  1. Susan Leemburg: Division of Vascular Neurology and Rehabilitation, Department of Neurology, University Hospital Zurich, Zurich, Switzerland.
  2. Tara Canonica: Division of Vascular Neurology and Rehabilitation, Department of Neurology, University Hospital Zurich, Zurich, Switzerland.
  3. Andreas Luft: Division of Vascular Neurology and Rehabilitation, Department of Neurology, University Hospital Zurich, Zurich, Switzerland. andreas.luft@usz.ch.

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.

References

  1. J Neurosci. 2012 Sep 19;32(38):13309-26 [PMID: 22993446]
  2. Brain Res Rev. 2007 Nov;56(1):27-78 [PMID: 17574681]
  3. Annu Rev Neurosci. 2007;30:259-88 [PMID: 17600522]
  4. J Neurosci. 2002 Aug 15;22(16):7225-33 [PMID: 12177217]
  5. PLoS One. 2009 Sep 17;4(9):e7082 [PMID: 19759902]
  6. Front Mol Neurosci. 2016 Jan 05;8:78 [PMID: 26778955]
  7. Behav Brain Res. 2011 Mar 1;217(2):354-62 [PMID: 21070820]
  8. Nature. 2010 Jul 22;466(7305):457-62 [PMID: 20651684]
  9. Synapse. 2005 Jun 1;56(3):166-9 [PMID: 15765533]
  10. Mol Neurobiol. 2005 Dec;32(3):205-16 [PMID: 16385137]
  11. Life Sci. 1979 Oct 8;25(15):1351-60 [PMID: 574606]
  12. Brain Res. 1998 Sep 14;805(1-2):169-80 [PMID: 9733960]
  13. Behav Brain Res. 2004 Dec 6;155(2):249-56 [PMID: 15364484]
  14. Brain Res. 2015 Dec 2;1628(Pt A):157-73 [PMID: 25446457]
  15. Nat Rev Neurosci. 2016 Mar;17(3):183-95 [PMID: 26865020]
  16. Pharmacol Biochem Behav. 1998 Sep;61(1):87-92 [PMID: 9715810]
  17. Synapse. 2009 Oct;63(10):823-35 [PMID: 19533625]
  18. Nature. 2012 Jan 18;482(7383):85-8 [PMID: 22258508]
  19. Behav Neurosci. 1997 Apr;111(2):369-80 [PMID: 9106676]
  20. J Neurosci. 2005 Jun 8;25(23):5553-62 [PMID: 15944383]
  21. J Neurosci. 2000 Mar 1;20(5):RC62 [PMID: 10684909]
  22. J Neurosci. 2003 Aug 20;23(20):7569-76 [PMID: 12930795]
  23. Neuroscience. 2007 Sep 7;148(3):623-32 [PMID: 17693029]
  24. Neuropsychopharmacology. 2005 Feb;30(2):330-8 [PMID: 15383830]
  25. Behav Brain Res. 2011 Jun 20;220(1):112-8 [PMID: 21295078]
  26. Exp Brain Res. 2015 May;233(5):1365-75 [PMID: 25633321]
  27. Behav Brain Res. 2012 Dec 1;235(2):150-7 [PMID: 22963991]
  28. J Neurochem. 1997 Jul;69(1):137-43 [PMID: 9202304]
  29. PLoS One. 2011 Jan 27;6(1):e16528 [PMID: 21304590]
  30. Elife. 2015 Sep 29;4:e09423 [PMID: 26417950]
  31. Cell. 2015 Jul 30;162(3):622-34 [PMID: 26232228]
  32. J Neurosci. 2000 May 15;20(10 ):3864-73 [PMID: 10804226]
  33. Brain Res Mol Brain Res. 2005 Jun 13;137(1-2):184-92 [PMID: 15950777]
  34. Nat Rev Neurosci. 2017 Feb;18(2):73-85 [PMID: 28053327]
  35. Neuron. 2010 Dec 9;68(5):815-34 [PMID: 21144997]
  36. Nat Rev Neurosci. 2004 Jun;5(6):483-94 [PMID: 15152198]
  37. Brain Res. 1978 Feb 24;142(2):249-67 [PMID: 24492]
  38. J Neurosci. 2011 Feb 16;31(7):2481-7 [PMID: 21325515]
  39. Brain Res Bull. 2015 Feb;111:9-19 [PMID: 25460109]
  40. J Pharmacol Exp Ther. 2005 Nov;315(2):648-57 [PMID: 16076936]
  41. Rev Neurosci. 2014;25(5):621-30 [PMID: 24887956]
  42. Neurosci Biobehav Rev. 2010 Apr;34(5):769-80 [PMID: 19914285]
  43. Brain Res Bull. 2006 Jan 15;68(4):233-48 [PMID: 16377429]
  44. Eur J Pharmacol. 2012 Aug 15;689(1-3):118-24 [PMID: 22659588]
  45. J Neurosci. 1981 Dec;1(12):1361-8 [PMID: 6172572]
  46. J Neurosci. 1999 May 15;19(10):3723-30 [PMID: 10234004]

MeSH Term

Animals
Behavior, Animal
Dopaminergic Neurons
Male
Microscopy, Fluorescence
Motor Skills
Proto-Oncogene Proteins c-fos
Rats
Rats, Long-Evans
Ventral Tegmental Area

Chemicals

Proto-Oncogene Proteins c-fos

Word Cloud

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