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.
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 at https://doi.org/10.6084/m9.figshare.c.4368464.v1.
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All anonymised behavioural data collected via the online task are freely available on the Open Science Framework website (http://osf.io/8mzyc/).
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/).
Wagenaar, W. A. My memory: a study of autobiographical memory over six years. Cogn. Psychol. 18, 225–252 (1986).
Ebbinghaus, H. Memory: a contribution to experimental psychology. Ann. Neurosci. 20, 155–156 (2013).
McGeoch, J. A. Forgetting and the law of disuse. Psychol. Rev. 39, 352–370 (1932).
Postman, L. in Psychology 3rd edn (eds Kling, J. W. & Riggs, L.) 1019–1132 (Holt, Rinehart and Winston, 1971).
Wixted, J. T. The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 55, 235–269 (2004).
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).
Richards, B. A. & Frankland, P. W. The persistence and transience of memory. Neuron 94, 1071–1084 (2017).
Hardt, O., Nader, K. & Nadel, L. Decay happens: the role of active forgetting in memory. Trends Cogn. Sci. 17, 111–120 (2013).
Reyna, V. F. & Brainerd, C. J. Fuzzy-trace theory: interim theory synthesis. Learn. Individ. Differ. 7, 1–75 (1995).
Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997).
Winocur, G. & Moscovitch, M. Memory transformation and systems consolidation. J. Int. Neuropsychol. Soc. 17, 766–780 (2011).
Sekeres, M. J., Winocur, G. & Moscovitch, M. The hippocampus and related neocortical structures in memory transformation. Neurosci. Lett. 680, 39–53 (2018).
Murphy, G. L. & Shapiro, A. M. Forgetting of verbatim information in discourse. Mem. Cognit. 22, 84–94 (1994).
Kintsch, W., Welsch, D., Schmalhofer, F. & Zimny, S. Sentence memory: a theoretical analysis. J. Mem. Lang. 159, 133–159 (1990).
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).
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).
Harlow, I. M. & Donaldson, D. I. Source accuracy data reveal the thresholded nature of human episodic memory. Psychon. Bull. Rev. 20, 318–325 (2013).
Harlow, I. M. & Yonelinas, A. P. Distinguishing between the success and precision of recollection. Memory 24, 114–127 (2016).
Richter, F. R., Cooper, R. A., Bays, P. M. & Simons, J. S. Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory. eLife 5, 1–18 (2016).
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. Neuropsychologia 119, 101–106 (2018).
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).
Schurgin, M. W., Wixted, J. T. & Brady, T. F. Psychophysical scaling reveals a unified theory of visual memory strength. Preprint at bioRxiv https://doi.org/10.1101/325472 (2018).
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).
Luck, S., Vogel, J. & Edward, K. The capacity of visual working memory for features and conjuctions. Nature 390, 279–281 (1997).
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).
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. Neuroimage 120, 298–308 (2015).
Cai, D., Kleeman, R. & Majda, A. A mathematical framework for quantifying predictability through relative entropy. Methods Appl. Anal. 9, 425–444 (2002).
Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).
Verdugo Lazo, A. C. G. & Rathie, P. N. On the entropy of continuous probability distributions. IEEE Trans. Inf. Theory 24, 120–122 (1978).
Bartlett, F. F. C Remembering: An Experimental and Social Study. (Cambridge Univ: 1932).
Ghosh, V. E. & Gilboa, A. What is a memory schema? A historical perspective on current neuroscience literature. Neuropsychologia 53, 104–114 (2014).
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).
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).
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).
Arpit, D. et al. A closer look at memorization in deep networks. Proc. 34th Internat. Conf. Mach. Learn. 70, 233–242 (2017).
Richter, F. R., Bays, P. M., Jeyarathnarajah, P. & Simons, J. S. Flexible updating of dynamic knowledge structures. Sci. Rep. 9, 2272 (2019).
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 at PsyArXiv https://doi.org/10.31234/osf.io/zeg95 (2018).
Richards, B. A. et al. Patterns across multiple memories are identified over time. Nat. Neurosci. 17, 981–986 (2014).
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).
Diamond, N. B., Armson, M. J. & Levine, B. The truth is out there: accuracy and detail in recall of verifiable real-world events. Preprint at PsyArXiv https://doi.org/10.31234/osf.io/ud63x (2019).
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).
Davis, R. L. & Zhong, Y. The biology of forgetting—a perspective. Neuron 95, 490–503 (2017).
Frankland, P. W., Köhler, S. & Josselyn, S. A. Hippocampal neurogenesis and forgetting. Trends Neurosci. 36, 497–503 (2013).
Ryan, T. J., Roy, D. S., Pignatelli, M., Arons, A. & Tonegawa, S. Engram cells retain memory under retrograde amnesia. Science 348, 1007–1013 (2015).
Roy, D. S., Muralidhar, S., Smith, L. M. & Tonegawa, S. Silent memory engrams as the basis for retrograde amnesia. Proc. Natl Acad. Sci. USA 114, E9972–E9979 (2017).
Tulving, E. Ecphoric processes in episodic memory. Philos. Trans. R. Soc. Lond. B 302, 361–371 (1983).
Tulving, E. Elements of Episodic Memory (Clarendon Press, 1983).
Frankland, P. W., Josselyn, S. A. & Köhler, S. The neurobiological foundation of memory retrieval. Nat. Neurosci. 22, 1576–1585 (2019).
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. Brain 136, 2474–2485 (2013).
Tompary, A., Zhou, W. & Davachi, L. Schematic memories develop quickly, but are not expressed unless necessary. Preprint at PsyArXiv https://doi.org/10.31234/osf.io/k4fea (2020).
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).
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).
Kumaran, D. What representations and computations underpin the contribution of the hippocampus to generalization and inference? Front. Hum. Neurosci. 6, 1–11 (2012).
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. B 372, 20160049 (2017).
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).
Mikolov, T., Chen, K., Corrado, G. & Dean, J. Efficient estimation of word representations in vector space. Preprint at https://arxiv.org/abs/1301.3781 (2013).
Rubin, D. C. & Wenzel, A. E. One hundred years of forgetting: a quantitative description of retention. Psychol. Rev. 103, 734–760 (1996).
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.
The authors declare no competing interests.
Peer review information Primary Handling Editor: Marike Schiffer.
Supplementary Figures, Supplementary Tables, Supplementary Methods and Supplementary References.
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).
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 Behav (2020). https://doi.org/10.1038/s41562-020-0888-8