The reach of reactivation: Effects of consciously triggered versus unconsciously triggered reactivation of associative memory.

Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE

Original Publication: Washington, DC : National Academy of Sciences

Learning* ; Memory Consolidation*/physiology; Humans ; Consciousness ; Wakefulness/physiology ; Sleep/physiology ; Inhibition, Psychological

Consolidating memories for long-term storage depends on reactivation. Reactivation occurs both consciously, during wakefulness, and unconsciously, during wakefulness and sleep. While considerable work has examined conscious awake and unconscious sleep reactivation, in this study, we directly compare the consequences of conscious and unconscious reactivation during wakefulness. Forty-one participants learned associations consisting of adjective-object-position triads. Objects were clustered into distinct semantic groups (e.g., fruits, vehicles) such that we could examine consequences of reactivation on semantically related memories. After an intensive learning protocol, we systematically reactivated some of the triads by presenting the adjective as a cue. Reactivation was done so that it was consciously experienced for some triads, and only unconsciously processed for others. Memory for spatial positions, the most distal part of the association, was affected by reactivation in a consciousness-dependent and memory-strength-dependent manner. Conscious reactivation resulted in weakening of semantically related memories that were strong initially, resonating with prior findings of retrieval-induced forgetting. Unconscious reactivation, on the other hand, selectively benefited weak reactivated memories, as previously shown for reactivation during sleep. Semantically linked memories were not impaired, but rather were integrated with the reactivated memory. These results taken together demonstrate that conscious and unconscious reactivation have qualitatively different consequences. Results support a consciousness-dependent inhibition account, whereby unconscious reactivation entails less inhibition than conscious reactivation, thus allowing more liberal spread of activation. Findings set the stage for additional exploration into the role of conscious experience in memory storage and structuring.
Competing Interests: Competing interests statement:The authors declare no competing interest.

Update of: bioRxiv. 2023 Jul 28:2023.07.26.546400. doi: 10.1101/2023.07.26.546400. (PMID: 37546839)
Comment in: Proc Natl Acad Sci U S A. 2024 Mar 26;121(13):e2402870121. doi: 10.1073/pnas.2402870121. (PMID: 38498730)

Sci Rep. 2017 Nov 10;7(1):15325. (PMID: 29127388)
Trends Cogn Sci. 2011 Aug;15(8):343-51. (PMID: 21764357)
Nat Neurosci. 2007 Jul;10(7):908-14. (PMID: 17558403)
Sleep. 2015 May 01;38(5):755-63. (PMID: 25515103)
Philos Trans R Soc Lond B Biol Sci. 2007 May 29;362(1481):857-75. (PMID: 17403642)
Psychol Sci. 2006 Mar;17(3):249-55. (PMID: 16507066)
Sci Rep. 2021 Jan 14;11(1):1383. (PMID: 33446812)
Trends Cogn Sci. 2013 Mar;17(3):142-9. (PMID: 23433937)
Nat Commun. 2017 Nov 3;8(1):1311. (PMID: 29101315)
Trends Cogn Sci. 2022 Sep;26(9):782-795. (PMID: 35842373)
Science. 1996 Sep 20;273(5282):1699-702. (PMID: 8781230)
Spat Vis. 1997;10(4):433-6. (PMID: 9176952)
Front Comput Neurosci. 2014 Nov 04;8:138. (PMID: 25408645)
Proc Natl Acad Sci U S A. 2007 May 1;104(18):7723-8. (PMID: 17449637)
Cereb Cortex. 2015 Oct;25(10):3994-4008. (PMID: 25477369)
Trends Cogn Sci. 2019 Sep;23(9):726-742. (PMID: 31358438)
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19591-6. (PMID: 24218550)
Conscious Cogn. 2012 Jun;21(2):953-60. (PMID: 22425537)
Nat Neurosci. 2001 Jul;4(7):752-8. (PMID: 11426233)
Nat Rev Neurosci. 2010 Feb;11(2):114-26. (PMID: 20046194)
Nature. 1997 Feb 6;385(6616):533-6. (PMID: 9020359)
Conscious Cogn. 2015 Sep;35:234-50. (PMID: 25704454)
J Exp Psychol Learn Mem Cogn. 2024 Feb;50(2):266-286. (PMID: 36265044)
Curr Biol. 2019 Sep 23;29(18):R906-R912. (PMID: 31550479)
Nat Rev Neurosci. 2011 Jan;12(1):17-30. (PMID: 21170072)
Learn Mem. 2023 Jan 31;30(2):36-42. (PMID: 36720637)
Psychol Sci. 2020 Jun;31(6):663-677. (PMID: 32384011)
Sleep Med Rev. 2009 Oct;13(5):305-8. (PMID: 19699665)
Neuron. 2010 Jan 28;65(2):280-90. (PMID: 20152133)
Trends Cogn Sci. 2002 Feb 1;6(2):93-102. (PMID: 15866193)
Sleep. 2016 May 01;39(5):1139-50. (PMID: 26856905)
Nat Neurosci. 2023 Aug;26(8):1429-1437. (PMID: 37429914)
Brain Struct Funct. 2019 Mar;224(2):713-726. (PMID: 30478610)
Trends Cogn Sci. 2019 Oct;23(10):876-890. (PMID: 31445780)
Psychol Bull. 2020 Mar;146(3):218-244. (PMID: 32027149)
Nat Commun. 2018 Sep 25;9(1):3920. (PMID: 30254219)
Neuron. 2017 Sep 27;96(1):228-241.e5. (PMID: 28957671)
Percept Psychophys. 2002 Jan;64(1):148-62. (PMID: 11916298)
Psychol Sci. 2010 Oct;21(10):1464-70. (PMID: 20807896)
J Neurosci. 2012 Mar 7;32(10):3453-61. (PMID: 22399768)
Cell Rep. 2023 Apr 25;42(4):112331. (PMID: 37014750)
Psychol Sci. 2007 Dec;18(12):1044-9. (PMID: 18031410)
Science. 2006 Dec 15;314(5806):1786-8. (PMID: 17170308)

R00 MH122663 United States MH NIMH NIH HHS

Keywords: consciousness; inhibition; memory consolidation; memory reactivation

Date Created: 20240226 Date Completed: 20240228 Latest Revision: 20240827

20240827

PMC10927514

10.1073/pnas.2313604121

38408248