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Dissociating memory accessibility and precision in forgetting

自然人类的性能变化ourvolume4,pages866–877 (2020)Cite this article

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Abstract

Forgetting involves the loss of information over time; however, we know little about what form this information loss takes. Do memories become less precise over time, or do they instead become less accessible? Here we assessed memory for word–location associations across four days, testing whether forgetting involves losses in precision versus accessibility and whether such losses are modulated by learning a generalizable pattern. We show that forgetting involves losses in memory accessibility with no changes in memory precision. When participants learned a set of related word–location associations that conformed to a general pattern, we saw a strong trade-off; accessibility was enhanced, whereas precision was reduced. However, this trade-off did not appear to be modulated by time or confer a long-term increase in the total amount of information maintained in memory. Our results place theoretical constraints on how models of forgetting and generalization account for time-dependent memory processes.

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The stage 1 protocol for this Registered Report was accepted in principle on 4 June 2019. The protocol, as accepted by the journal, can be found athttps://doi.org/10.6084/m9.figshare.c.4368464.v1.

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Fig. 1: Schematic of the experimental procedure.
Fig. 2: Memory performance by condition.
Fig. 3: Model-derived probability estimates for each type of the subjective memory judgement.
Fig. 4: Kullback–Leibler divergence by condition.

Data availability

All anonymised behavioural data collected via the online task are freely available on the Open Science Framework website (http://osf.io/8mzyc/).

Code availability

All HTML, PHP and MATLAB scripts used to run the experimental task and analyse the data are freely available on the Open Science Framework website (http://osf.io/8mzyc/).

References

  1. Wagenaar, W. A. My memory: a study of autobiographical memory over six years.Cogn. Psychol.18, 225–252 (1986).

    Google Scholar

  2. Ebbinghaus, H. Memory: a contribution to experimental psychology.Ann. Neurosci.20, 155–156 (2013).

    PubMedGoogle Scholar

  3. McGeoch, J. A. Forgetting and the law of disuse.Psychol. Rev.39, 352–370 (1932).

    Google Scholar

  4. Postman, L. inPsychology3rd edn (eds Kling, J. W. & Riggs, L.) 1019–1132 (Holt, Rinehart and Winston, 1971).

  5. Wixted, J. T. The psychology and neuroscience of forgetting.Annu. Rev. Psychol.55, 235–269 (2004).

    PubMedGoogle Scholar

  6. Sadeh, T., Ozubko, J. D., Winocur, G. & Moscovitch, M. How we forget may depend on how we remember.Trends Cogn. Sci.18, 26–36 (2014).

    PubMedGoogle Scholar

  7. Richards, B. A. & Frankland, P. W. The persistence and transience of memory.Neuron94, 1071–1084 (2017).

    CASPubMedGoogle Scholar

  8. Hardt, O., Nader, K. & Nadel, L. Decay happens: the role of active forgetting in memory.Trends Cogn. Sci.17, 111–120 (2013).

    PubMedGoogle Scholar

  9. Reyna, V. F. & Brainerd, C. J. Fuzzy-trace theory: interim theory synthesis.Learn. Individ. Differ.7, 1–75 (1995).

    Google Scholar

  10. Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex.Curr. Opin. Neurobiol.7, 217–227 (1997).

    CASPubMedGoogle Scholar

  11. Winocur, G. & Moscovitch, M. Memory transformation and systems consolidation.J. Int. Neuropsychol. Soc.17, 766–780 (2011).

    PubMedGoogle Scholar

  12. Sekeres, M. J., Winocur, G. & Moscovitch, M. The hippocampus and related neocortical structures in memory transformation.Neurosci. Lett.680, 39–53 (2018).

    CASPubMedGoogle Scholar

  13. Murphy, G. L. & Shapiro, A. M. Forgetting of verbatim information in discourse.Mem. Cognit.22, 84–94 (1994).

    Google Scholar

  14. Kintsch, W., Welsch, D., Schmalhofer, F. & Zimny, S. Sentence memory: a theoretical analysis.J. Mem. Lang.159, 133–159 (1990).

    Google Scholar

  15. Sekeres, M. J. et al. Recovering and preventing loss of detailed memory: differential rates of forgetting for detail types in episodic memory.Learn. Mem.23, 72–82 (2016).

    PubMedPubMed CentralGoogle Scholar

  16. Furman, O., Hasson, U., Davachi, L., Dorfman, N. & Dudai, Y. They saw a movie: long-term memory for an extended audiovisual narrative.Learn. Mem.14, 457–467 (2007).

    PubMedPubMed CentralGoogle Scholar

  17. Harlow, I. M. & Donaldson, D. I. Source accuracy data reveal the thresholded nature of human episodic memory.Psychon. Bull. Rev.20, 318–325 (2013).

    PubMedGoogle Scholar

  18. Harlow, I. M. & Yonelinas, A. P. Distinguishing between the success and precision of recollection.Memory24, 114–127 (2016).

    PubMedGoogle Scholar

  19. Richter, F. R., Cooper, R. A., Bays, P. M. & Simons, J. S. Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory.eLife5, 1–18 (2016).

    Google Scholar

  20. Nilakantan, A. S., Bridge, D. J., VanHaerents, S. & Voss, J. L. Distinguishing the precision of spatial recollection from its success: evidence from healthy aging and unilateral mesial temporal lobe resection.Neuropsychologia119, 101–106 (2018).

    PubMedPubMed CentralGoogle Scholar

  21. Nilakantan, A. S., Bridge, D. J., Gagnon, E. P., VanHaerents, S. A. & Voss, J. L. Stimulation of the posterior cortical–hippocampal network enhances precision of memory recollection.Curr. Biol.27, 465–470 (2017).

    CASPubMedPubMed CentralGoogle Scholar

  22. Wixted Schurgin, m . W。,j . t . &布雷迪,t . f .心理学hophysical scaling reveals a unified theory of visual memory strength. Preprint atbioRxivhttps://doi.org/10.1101/325472(2018).

  23. Sun, S. Z. et al. Erasing and blurring memories: The differential impact of interference on separate aspects of forgetting.J. Exp. Psychol. Gen.146, 1606–1630 (2017).

    PubMedGoogle Scholar

  24. Luck, S., Vogel, J. & Edward, K. The capacity of visual working memory for features and conjuctions.Nature390, 279–281 (1997).

    CASPubMedGoogle Scholar

  25. Bays, P. M., Catalao, R. F. G. & Husain, M. The precision of visual working memory is set by allocation of a shared resource.J. Vis.9, 7.1–7.11 (2009).

    Google Scholar

  26. Murray, J. G., Howie, C. A. & Donaldson, D. I. The neural mechanism underlying recollection is sensitive to the quality of episodic memory: event related potentials reveal a some-or-none threshold.Neuroimage120, 298–308 (2015).

    PubMedGoogle Scholar

  27. Cai, D., Kleeman, R. & Majda, A. A mathematical framework for quantifying predictability through relative entropy.Methods Appl. Anal.9, 425–444 (2002).

    Google Scholar

  28. Shannon, C. E. A mathematical theory of communication.Bell Syst. Tech. J.27, 379 - 423(1948)。

    Google Scholar

  29. Verdugo Lazo, A. C. G. & Rathie, P. N. On the entropy of continuous probability distributions.IEEE Trans. Inf. Theory24, 120 - 122(1978)。

    Google Scholar

  30. Bartlett, F. F. CRemembering: An Experimental and Social Study. (Cambridge Univ: 1932).

  31. Ghosh, V. E. & Gilboa, A. What is a memory schema? A historical perspective on current neuroscience literature.Neuropsychologia53, 104–114 (2014).

    PubMedGoogle Scholar

  32. Van Kesteren, M. T. R., Ruiter, D. J., Fernández, G. & Henson, R. N. How schema and novelty augment memory formation.Trends Neurosci.35, 211–219 (2012).

    PubMedGoogle Scholar

  33. McClelland, J. L., McNaughton, B. L. & O’Reilly, R. C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.Psychol. Rev.102, 419–457 (1995).

    PubMedGoogle Scholar

  34. Kan, I. P., Alexander, M. P. & Verfaellie, M. Contribution of prior semantic knowledge to new episodic learning in amnesia.J. Cogn. Neurosci.21, 938–944 (2009).

    PubMedPubMed CentralGoogle Scholar

  35. Arpit, D. et al. A closer look at memorization in deep networks.Proc. 34th Internat. Conf. Mach. Learn.70, 233–242 (2017).

  36. Richter, F. R., Bays, P. M., Jeyarathnarajah, P. & Simons, J. S. Flexible updating of dynamic knowledge structures.Sci. Rep.9, 2272 (2019).

    PubMedPubMed CentralGoogle Scholar

  37. Brady, T. F., Schacter, D. L. & Alvarez, G. A. The adaptive nature of false memories is revealed by gist-based distortion of true memories. Preprint atPsyArXivhttps://doi.org/10.31234/osf.io/zeg95(2018).

  38. Richards, B. A. et al. Patterns across multiple memories are identified over time.Nat. Neurosci.17, 981–986 (2014).

    CASPubMedGoogle Scholar

  39. Mack, M. L., Preston, A. R. & Love, B. C. Decoding the brain’s algorithm for categorization from its neural implementation.Curr. Biol.23, 2023–2027 (2013).

    CASPubMedGoogle Scholar

  40. Diamond, N. B., Armson, M. J. & Levine, B. The truth is out there: accuracy and detail in recall of verifiable real-world events. Preprint atPsyArXivhttps://doi.org/10.31234/osf.io/ud63x(2019).

  41. Joensen, B. H., Gaskell, M. G. & Horner, A. J. United we fall: all-or-none forgetting of complex episodic events.J. Exp. Psychol. Gen.149, 230–248 (2020).

    PubMedGoogle Scholar

  42. Davis, R. L. & Zhong, Y. The biology of forgetting—a perspective.Neuron95, 490–503 (2017).

    CASPubMedPubMed CentralGoogle Scholar

  43. Frankland, P. W., Köhler, S. & Josselyn, S. A. Hippocampal neurogenesis and forgetting.Trends Neurosci.36, 497–503 (2013).

    CASPubMedGoogle Scholar

  44. Ryan, T. J., Roy, D. S., Pignatelli, M., Arons, A. & Tonegawa, S. Engram cells retain memory under retrograde amnesia.Science3481007 - 1013 (2015).

    CASPubMedPubMed CentralGoogle Scholar

  45. Roy, D. S., Muralidhar, S., Smith, L. M. & Tonegawa, S. Silent memory engrams as the basis for retrograde amnesia.Proc. Natl Acad. Sci. USA114, E9972–E9979 (2017).

    CASPubMedGoogle Scholar

  46. Tulving, E. Ecphoric processes in episodic memory.Philos. Trans. R. Soc. Lond. B302, 361–371 (1983).

    Google Scholar

  47. Tulving, E.Elements of Episodic Memory(Clarendon Press, 1983).

  48. Frankland, P. W., Josselyn, S. A. & Köhler, S. The neurobiological foundation of memory retrieval.Nat. Neurosci.22, 1576–1585 (2019).

    CASPubMedPubMed CentralGoogle Scholar

  49. Pertzov, Y. et al. Binding deficits in memory following medial temporal lobe damage in patients with voltage-gated potassium channel complex antibody-associated limbic encephalitis.Brain136, 2474–2485 (2013).

    PubMedPubMed CentralGoogle Scholar

  50. Tompary, A., Zhou, W. & Davachi, L. Schematic memories develop quickly, but are not expressed unless necessary. Preprint atPsyArXivhttps://doi.org/10.31234/osf.io/k4fea(2020).

  51. Kumaran, D., Hassabis, D. & McClelland, J. L. What learning systems do intelligent agents need? Complementary learning systems theory updated.Trends Cogn. Sci.20, 512–534 (2016).

    PubMedGoogle Scholar

  52. Kumaran, D. & McClelland, J. L. Generalization through the recurrent interaction of episodic memories: A model of the hippocampal system.Psychol. Rev.119, 573–616 (2012).

    PubMedPubMed CentralGoogle Scholar

  53. Kumaran, D. What representations and computations underpin the contribution of the hippocampus to generalization and inference?Front. Hum. Neurosci.6, 1–11 (2012).

    Google Scholar

  54. Schapiro, A. C., Turk-Browne, N. B., Botvinick, M. M. & Norman, K. A. Complementary learning systems within the hippocampus: A neural network modelling approach to reconciling episodic memory with statistical learning.Philos. Trans. R. Soc. Lond. B372, 20160049 (2017).

    Google Scholar

  55. van Heuven, W. J. B., Mandera, P., Keuleers, E. & Brysbaert, M. SUBTLEX-UK: a new and improved word frequency database for British English.Q. J. Exp. Psychol.67, 1176–1190 (2014).

    Google Scholar

  56. Mikolov, T., Chen, K., Corrado, G. & Dean, J. Efficient estimation of word representations in vector space. Preprint athttps://arxiv.org/abs/1301.3781(2013).

  57. Rubin, D. C. & Wenzel, A. E. One hundred years of forgetting: a quantitative description of retention.Psychol. Rev.103, 734–760 (1996).

    Google Scholar

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Acknowledgements

We thank S. Mod, L. Begic, T. Houldridge and T. Maltby for help with collecting the laboratory-based pilot data. A.J.H. is funded by the Wellcome Trust (204277/Z/16/Z) and the Economic and Social Research Council (ES/R007454/1). B.A.R. is funded by a Learning in Machines and Brains Fellowship from the Canadian Institute for Advanced Research and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (RGPIN-2014-04947). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Department of Psychology, University of York, York, UK

    Sam C. Berens & Aidan J. Horner

  2. School of Psychology, University of Sussex, Brighton, UK

    Sam C. Berens

  3. Mila, Montreal, Quebec, Canada

    Blake A. Richards

  4. Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec, Canada

    Blake A. Richards

  5. School of Computer Science, McGill University, Montreal, Quebec, Canada

    Blake A. Richards

  6. Learning in Machines and Brains Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada

    Blake A. Richards

  7. York Biomedical Research Institute, University of York, York, UK

    Aidan J. Horner

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Contributions

S.C.B., B.A.R. and A.J.H. contributed to research design and provided input on the manuscript. S.C.B. and A.J.H. wrote the manuscript and developed the analysis pipeline. S.C.B. coded the experimental tasks, derived the experimental metrics and implemented the statistical analyses.

Corresponding authors

Correspondence toSam C. BerensorAidan J. Horner.

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The authors declare no competing interests.

Additional information

Peer review informationPrimary Handling Editor: Marike Schiffer.

Supplementary information

Supplementary Information

Supplementary Figures, Supplementary Tables, Supplementary Methods and Supplementary References.

Reporting Summary

Supplementary Software 1

A ZIP archive containing MATLAB functions and R scripts necessary for running each analysis reported in the manuscript and reproducing all the figures. This archive has 5 subdirectories ’#_Dependencies’ (file dependencies), ‘0_PreReg’ (pre-registered analyses), ‘1_Sujective’ (exploratory analyses of subjective report data), ‘2_ExNeither’ (exploratory analysis that excluded ‘Neither responses’), and ‘3_Kld’ (exploratory analyses on Kullback–Leibler divergence statistics).

Supplementary Software 1

A ZIP archive containing all the HTML, JavaScript and PHP files required for running the experimental task on a MySQL enabled webserver. ‘index.php’ is the first page that naïve participants are served.

Supplementary Data 1

A Microsoft Excel Workbook with three different sheets. Sheet 1 (titled ‘ManmadeWords’) lists all the word stimuli in ‘manmade object’ semantic category. Sheet 2 (titled ‘NaturalWords’) lists all the word stimuli in ‘natural object’ semantic category. Sheet 3 (titled ‘MainDataset’) contains all the anonymised data included in the final sample.

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Berens, S.C., Richards, B.A. & Horner, A.J. Dissociating memory accessibility and precision in forgetting.Nat Hum Behav4, 866–877 (2020). https://doi.org/10.1038/s41562-020-0888-8

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