Negative reinforcement impairs overnight memory consolidation.

Andrew W Stamm, Nam D Nguyen, Benjamin J Seicol, Abigail Fagan, Angela Oh, Michael Drumm, Maureen Lundt, Robert Stickgold, Erin J Wamsley
Author Information
  1. Andrew W Stamm: Department of Psychiatry, Harvard Medical School, Boston, Massachusetts 02215, USA.
  2. Nam D Nguyen: Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215, USA.
  3. Benjamin J Seicol: Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215, USA.
  4. Abigail Fagan: University of Rochester, Rochester, New York 14604, USA.
  5. Angela Oh: Harvard University, Cambridge, Massachusetts 02138, USA.
  6. Michael Drumm: Harvard University, Cambridge, Massachusetts 02138, USA.
  7. Maureen Lundt: Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215, USA.
  8. Robert Stickgold: Department of Psychiatry, Harvard Medical School, Boston, Massachusetts 02215, USA Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215, USA.
  9. Erin J Wamsley: Department of Psychiatry, Harvard Medical School, Boston, Massachusetts 02215, USA Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, Massachusetts 02215, USA erin.wamsley@furman.edu.

Abstract

Post-learning sleep is beneficial for human memory. However, it may be that not all memories benefit equally from sleep. Here, we manipulated a spatial learning task using monetary reward and performance feedback, asking whether enhancing the salience of the task would augment overnight memory consolidation and alter its incorporation into dreaming. Contrary to our hypothesis, we found that the addition of reward impaired overnight consolidation of spatial memory. Our findings seemingly contradict prior reports that enhancing the reward value of learned information augments sleep-dependent memory processing. Given that the reward followed a negative reinforcement paradigm, consolidation may have been impaired via a stress-related mechanism.

References

  1. J Exp Psychol Learn Mem Cogn. 2009 Nov;35(6):1586-93 [PMID: 19857029]
  2. Sleep Med Rev. 2006 Feb;10(1):49-62 [PMID: 16376591]
  3. Nat Neurosci. 2002 Jul;5(7):677-81 [PMID: 12032542]
  4. J Neurosci. 2009 Aug 26;29(34):10512-9 [PMID: 19710304]
  5. Hippocampus. 2008;18(8):844-51 [PMID: 18493970]
  6. Neuron. 2002 Jul 3;35(1):205-11 [PMID: 12123620]
  7. Nat Neurosci. 2000 Dec;3(12):1237-8 [PMID: 11100141]
  8. Science. 1994 Jul 29;265(5172):676-9 [PMID: 8036517]
  9. Psychoneuroendocrinology. 2001 Apr;26(3):307-17 [PMID: 11166493]
  10. Neuron. 2009 Feb 26;61(4):496-8 [PMID: 19249269]
  11. PLoS One. 2013 Oct 09;8(10):e75326 [PMID: 24130703]
  12. Psychol Sci. 2008 Aug;19(8):781-8 [PMID: 18816285]
  13. Physiol Behav. 2013 Oct 2;122:163-71 [PMID: 24012698]
  14. Nat Neurosci. 2013 Feb;16(2):139-45 [PMID: 23354387]
  15. PLoS One. 2007 Apr 18;2(4):e376 [PMID: 17440612]
  16. PLoS One. 2012;7(8):e43426 [PMID: 22916259]
  17. PLoS One. 2011;6(11):e27139 [PMID: 22110606]
  18. Neuroreport. 1999 Sep 9;10(13):2741-7 [PMID: 10511433]
  19. Neurobiol Learn Mem. 2006 Sep;86(2):241-7 [PMID: 16647282]
  20. Curr Biol. 2010 May 11;20(9):850-5 [PMID: 20417102]
  21. J Neurosci. 1999 May 15;19(10):4090-101 [PMID: 10234037]
  22. J Cogn Neurosci. 2011 Dec;23(12):3703-12 [PMID: 21736452]
  23. J Neurosci. 2013 Apr 10;33(15):6672-8 [PMID: 23575863]
  24. Cereb Cortex. 2015 Mar;25(3):646-57 [PMID: 24072888]
  25. Brain Res Bull. 2006 Dec 11;71(1-3):4-9 [PMID: 17113921]
  26. Neurobiol Learn Mem. 2012 Sep;98(2):188-96 [PMID: 22732649]
  27. Sleep. 2013 Jul 01;36(7):1051-1057 [PMID: 23814342]
  28. Trends Cogn Sci. 2007 Oct;11(10):442-50 [PMID: 17905642]
  29. Hippocampus. 2012 May;22(5):1154-63 [PMID: 21739522]
  30. Nat Neurosci. 2007 May;10(5):540-2 [PMID: 17453055]
  31. J Cogn Neurosci. 1997 Jul;9(4):534-47 [PMID: 23968216]
  32. Proc Natl Acad Sci U S A. 2006 May 2;103(18):7124-9 [PMID: 16636288]
  33. Learn Mem. 2010 Sep 30;17(10):522-30 [PMID: 20884754]
  34. PLoS One. 2011;6(7):e21737 [PMID: 21799746]
  35. J Clin Psychol. 2002 Jan;58(1):61-75 [PMID: 11748597]
  36. Memory. 2006 Jan;14(1):1-16 [PMID: 16423737]
  37. Nat Neurosci. 2007 Jan;10(1):100-7 [PMID: 17173043]
  38. Neuron. 2004 Oct 28;44(3):535-45 [PMID: 15504332]
  39. Front Neurol. 2013 Sep 30;4:143 [PMID: 24137153]
  40. Psychoneuroendocrinology. 1999 Apr;24(3):313-31 [PMID: 10101736]
  41. Front Integr Neurosci. 2012 Nov 21;6:108 [PMID: 23181013]
  42. Proc Natl Acad Sci U S A. 2007 May 1;104(18):7723-8 [PMID: 17449637]
  43. Learn Mem. 2007 Jan-Feb;14(1):109-16 [PMID: 17272656]
  44. Biol Psychiatry. 2002 Apr 1;51(7):575-82 [PMID: 11950459]
  45. J Neurosci. 2011 Feb 2;31(5):1563-9 [PMID: 21289163]
  46. Learn Mem. 2010 Jun 25;17(7):332-6 [PMID: 20581255]

Grants

  1. 8UL1TR000170-05/NCATS NIH HHS
  2. 8KL2TR000168-05/NCATS NIH HHS
  3. R01-MH48832/NIMH NIH HHS
  4. KL2 TR000168/NCATS NIH HHS
  5. UL1 TR000170/NCATS NIH HHS
  6. R01 MH048832/NIMH NIH HHS

MeSH Term

Adolescent
Adult
Humans
Memory
Reinforcement, Psychology
Reward
Sleep
Spatial Learning
Young Adult

Word Cloud

Created with Highcharts 10.0.0memoryrewardconsolidationovernightsleepmayspatialtaskenhancingimpairedreinforcementPost-learningbeneficialhumanHowevermemoriesbenefitequallymanipulatedlearningusingmonetaryperformancefeedbackaskingwhethersalienceaugmentalterincorporationdreamingContraryhypothesisfoundadditionfindingsseeminglycontradictpriorreportsvaluelearnedinformationaugmentssleep-dependentprocessingGivenfollowednegativeparadigmviastress-relatedmechanismNegativeimpairs

Similar Articles

Cited By