Tracking the relation between gist and item memory over the course of long-term memory consolidation

  1. Tima Zeng
  2. Alexa Tompary
  3. Anna C Schapiro
  4. Sharon L Thompson-Schill

  • Curated by eLife

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    Evaluation Summary:

    This paper is of interest to psychologists and neuroscientist investigating systems memory consolidation. It describes an experimental protocol that allows precise, quantitative behavioural measurements to assess the development and interactions of item and gist memory traces over extended time periods. The study design and hypotheses are elegant and bring together ideas from several other fields of cognitive psychology (working memory, category learning). However, additional analyses, and in particular, comparison of some simple computational models, are needed before the conclusions are justified.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)

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Abstract

Our experiences in the world support memories not only of specific episodes but also of the generalities (the ‘gist’) across related experiences. It remains unclear how these two types of memories evolve and influence one another over time. In two experiments, 173 human participants encoded spatial locations from a distribution and reported both item memory (specific locations) and gist memory (center for the locations) across 1–2 months. Experiment 1 demonstrated that after 1 month, gist memory was preserved relative to item memory, despite a persistent positive correlation between them. Critically, item memories were biased toward the gist over time. Experiment 2 showed that a spatial outlier item changed this relationship and that the extraction of gist is sensitive to the regularities of items. Our results suggest that the gist starts to guide item memories over longer durations as their relative strengths change.

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  1. eLife

    Evaluation Summary:

    This paper is of interest to psychologists and neuroscientist investigating systems memory consolidation. It describes an experimental protocol that allows precise, quantitative behavioural measurements to assess the development and interactions of item and gist memory traces over extended time periods. The study design and hypotheses are elegant and bring together ideas from several other fields of cognitive psychology (working memory, category learning). However, additional analyses, and in particular, comparison of some simple computational models, are needed before the conclusions are justified.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)

  2. eLife

    Reviewer #1 (Public Review):

    Zeng and colleagues present an interesting and timely exposition of how memory for items and generalities across related experiences are formed and influence each other. Across two carefully designed longitudinal studies spanning 1-2 months, the authors integrate insights from ensemble perception research to develop a novel landmark learning paradigm in which a set of landmarks are clustered together. Participants were required to learn the specific location of each landmark (item memory) as well as the spatial centre of the locations (reported gist). Leveraging hierarchical clustering models, the authors computed a gist-based bias measurement, enabling them to comment on the extent to which gist memory influences memory for specific items, as well as an index of estimated centre assembled from the retrieval of individual items. This enabled the authors to establish the amount of gist information available in item memories, and to tease apart the direction of the relationship between item and gist memory. I particularly appreciated Study 2's exploration of how the presence of an "outlier" item in spatial location impacts the gist and the relationship between item and gist representations from Study 1. This innovative approach allowed them to determine the extent to which the gist is robust against outlier items over time.

    Overall, I enjoyed reading this manuscript. It elegantly addresses an important and as yet unresolved question in cognitive science, namely the extent to which gist representations become independent of individual item memories as they are extracted during encoding and how this relationship potentially changes over time. The inclusion of a longitudinal dimension further enables us to understand something of the temporality of consolidation over short versus longer time periods. The manuscript is very well written, the experimental studies have been meticulously conducted using a novel interdisciplinary approach, limitations are appropriately acknowledged, and the conclusions drawn are highly appropriate and measured. I believe this study will make a very nice contribution to the memory literature and will certainly spur new lines of enquiry in this field.

  3. eLife

    Reviewer #2 (Public Review):

    It is often said that the amount of information humans can commit to long-term memory is essentially unlimited. However, this large storage capacity partly rests on our ability to compress new information before and during memory consolidation. One way to achieve such compression is by storing the common denominator of related experiences, which is often referred to as gist memory. During later recall, the brain is thought to deduce individual memories from the stored gist representation, rather than reading them out one by one. This not only reduces the memory footprint associated with learning, it also supports adaptive generalization of learning to novel situations.

    Zeng and colleagues address two important questions regarding gist memory: First, how do gist memory traces develop over time in comparison to memory traces for individual items? And second, how do the two classes of memory traces influence each other?

    The authors developed an experimental protocol in which healthy participants learn the association between landmark labels (e.g. university, park, restaurant) and abstract locations on a computer screen. Memory is subsequently measured in terms of the precision with which participants are able to indicate the learned locations, as well as their geometric center (i.e., the gist location).

    A major strength of this approach is that it allows for precise, quantitative assessments of item and gist memory, and how they influence each other. On the other hand, the abstract nature of the task makes it difficult to generalize the results to other forms of gist memory. Moreover, gist memory is explicitly assessed directly after initial learning, which does not allow for clear conclusions as to whether similar memory traces would have developed spontaneously. Nevertheless, the protocol represents a valuable tool for studying the interaction of related memory traces over time.

    The authors performed two experiments using this task. In the first experiment, they show that gist memory is more stable over one month compared to item memory; and that gist and item memory are positively related across all measured time-points (i.e., after 24 hours, one week, and one month). However, the nature of this positive correlation changes over time, with gist memory biasing item memory only after one month. The results of a second experiment corroborate these conclusions. They additionally indicate that outlier items (i.e., landmarks that are spatially distant from the cluster of all other landmarks) affect explicit, but not implicit gist memory, with only the latter biasing memories for individual items. Taken together, these results corroborate the notion that the importance of gist memories in guiding recall increases over time. Importantly, the data also provide an estimate of the relevant time window, i.e. between one week and one month after learning.

    My only major concern is that the experimental task provides a rather restricted view of gist memory. Thus, it remains unclear what the results mean for other kinds of gist memory, both visual and otherwise. The authors discuss this point on p.16 and offer some interesting speculations. However, the main problem I see is that memory for gist locations may reflect a combination of basic perceptual strategies (as acknowledged by the authors in their references to ensemble perception) and the demand characteristics of the task. This issue is most prominently seen in the difference between the effects for global and local centers observed in Experiment 2. Here, the instruction to explicitly recall the center is what may have created (or at least emphasized) the memory for the global center in the first place. More generally, the fact that gist memory was tested first and early on after learning may have changed the associated memory trace, making it difficult to generalize these findings to cases in which gist memories emerge spontaneously. While this may be the price to pay for precise, quantitative error and bias measures of errors, the authors should discuss these limitations in more detail.

  4. eLife

    Reviewer #3 (Public Review):

    A fundamental puzzle in human memory has been whether we retain individual experiences, and extract their gist by pooling over those experiences only when the gist is needed, or whether we also store a separate representation of the gist (regularities). This study uses locations of landmarks on a screen to argue that such a gist representation (the central tendency of the 2D locations of landmarks) is extracted gradually over time during memory consolidation, i.e, over a period between one day and a month after initial encoding of the landmark locations. Furthermore, the study suggests that this gist representation is not influenced by atypical locations, suggesting it is more than the simple average of all item memories, and that atypical stimuli may be encoded and/or retrieved separately.

    I think it would really improve the paper if the authors could compare a number of simple computational models, and show the model corresponding to their favoured conclusion (i.e, that a separate gist representation increases its influence on memory over time) is the only one that is consistent with their data. Ideally, this would entail quantitative fitting of parametrised models, but failing that, it might be sufficient to demonstrate qualitatively that certain models can never explain critical results (like the bias measure above, or the effect of an outlier). For example, I presume that an item-only model in which random noise (in both x,y directions) increased with delay could explain their first result of a greater effect of delay on reported item error (Ir) than Gr? But is this model consistent with their regression results, and most importantly, could it never reproduce their bias results?

    Another concern is whether the same results would hold if participants' representation of gist (Gr) were more than the simple average of their reported item locations (Ge). For example, would there be any consequences for the authors' conclusions if some 2D locations were represented more accurately than others - e.g, one might expect the location of landmarks close to the edge of the screen to be stored more accurately than ones closer to the centre of the screen (which could be tested by whether edge locations need fewer training trials?). I appreciate that locations are trained to the same criterion, but it is nonetheless possible that some representations are still more precisely encoded than others even after such criterion-training. Then if participants' reported centre were the weighted average of the reported item locations, weighted by each location's remembered precision, could that affect the authors' bias measure? I appreciate that this would not explain why the difference between reported and true centre changes over retention interval, but if one allowed location and precision information to decay at different rates, could this cause such an interaction with retention interval? This could be another model to simulate?

    It is unfortunate that the authors did not counterbalance the order of item and gist memory tests. They do consider this limitation in the Discussion, and note that any additive effect of test order would not explain the interaction between memory type and delay, but of course the presence of nonlinear/multiplicative effects (e.g, floor/ceiling effects) means it is not sufficient to conclude that their results could not depend on test order, i.e, it is always better to empirically test generalisation by running the other counterbalancing. This is particularly important here, where there are good a priori, theoretical reasons why test order might matter, e.g., shift people from strategies based on retrieving items or retrieving gist, depending on what type of memory is probed first. So while the authors state that this could be tested in future studies, the paper would be stronger if the authors could run this counterbalancing themselves and show the same results, so that future researchers do not waste time trying to replicate effects that turn out to be conditional on test order.

  5. Version published to 10.7554/elife.65588 on eLife
  6. Version published to 10.1101/2021.01.05.425378v1 on bioRxiv