Retrieval as a fast route to memory consolidation

Lead Research Organisation: University of Birmingham
Department Name: School of Psychology

Abstract

Human long-term memory has an astonishing capacity to store information about our own past experiences (episodic memory) as well as general knowledge (semantic memory). One of the big challenges in psychology is to understand what makes a memory last, i.e. why some experiences are easily remembered after days, weeks or even years, while other experiences fade and are ultimately forgotten.

The aim of this project is to investigate the role that active remembering plays in stabilizing newly acquired memories. Previous research has shown that remembering can protect memories against forgetting, such that experiences that are repeatedly retrieved after initial acquisition become more robust and more accessible in the long term. For example, in a recent study participants learned English-Swahili vocabulary pairs (e.g. "tomato - nyanya") and were then given the opportunity to practice the pairs, either by extra study ("tomato - nyanya") or by extra testing ("tomato - ?"). After one week, the vocabulary practiced by extra testing was retained 50% better than the vocabulary practiced by extra study. This striking memory improvement through retrieval ("testing effect") stands in sharp contrast to common classroom practice, where tests are typically used to measure learning success, rather than to enhance learning success. Interestingly, the study on vocabulary learning found that even university students are largely unaware of the memory-boosting effects of retrieval.

Surprisingly little is known about why retrieval has such a strong beneficial effect on memory. This project is aimed at investigating the neurocognitive mechanisms underlying the testing effect. All experiments are based on the central idea that memory traces change each time they are actively retrieved. Previous research has shown that the brain repeatedly "replays" newly acquired information during sleep or periods of awake rest after learning. Such offline reactivation seems crucial for the long-term stabilization (consolidation) of new memories. The current project will test the novel hypothesis that active retrieval mimics the changes that occur via offline consolidation, including making memory representations more semantic, less context-dependent, and more robust to interference. The experiments use an innovative combination of established and novel behavioural methods, as well as state-of-the-art pattern analysis of neuroimaging data, the latter being particularly well suited to track online the reactivation of individual memories in the brain.

The basic design used in all experiments is similar to the above vocabulary study. Participants will be given lists of materials to study once. They then receive i) no further practice, ii) practice by extra study, or iii) practice by extra testing. Retention of the materials will be assessed either immediately or after one week. The first set of experiments will explore whether visual and verbal materials equally benefit from testing. The second set of experiments will behaviourally test the central hypothesis that retrieval produces consolidation-like effects on memories. If retrieval mimics consolidation, it should have beneficial effects on some aspects of the learned information (e.g. semantic content), but detrimental effects on other aspects (e.g. contextual information). The final set of experiments uses functional magnetic resonance imaging (fMRI) to directly observe how the neural patterns that represent an individual memory change with repeated recall, and how these neural changes predict enhanced memory on a delayed test. Together, the results from these studies will advance our understanding of how active retrieval shapes and strengthens long-term memories. From an applied perspective, the results will help to identify the conditions under which repeated testing is useful in practice (e.g. in educational settings, or to boost memory in ageing populations).

Planned Impact

The proposed work addresses the central question in memory research on how repeated testing changes newly acquired memory traces and leads to enhanced long-term retention. The project is basic experimental in nature, and its primary impact will thus be on the field of basic psychological and neuroscientific research on long-term memory. Academics in these fields will benefit from the innovative framework of this project, which introduces a new theoretical perspective on retrieval-mediated learning, generating novel predictions and findings to inform theories of human memory. The project also uses an innovative methodological approach that has the potential to methodologically advance the field.

Second, the research on retrieval-mediated learning has a high potential to be applied to educational contexts. Therefore, the second group expected to benefit from the project are those working in the educational sector, be it policy makers in the Department for Education, or teachers of students at all age classes. Prior research has shown that teachers and students are mostly unaware of the memory-enhancing effects of testing. The educational sector will thus globally benefit from enhanced awareness of this research. More specifically, the project addresses questions of how testing improves memory, and which types of learning materials can benefit from this improvement. This information is highly relevant for teachers and policy makers alike, particularly with respect to the development of educational materials.

Third, there has always been a broad interest in memory research from the general public. This interest has increased in recent years, partly as a consequence of concerns about the health and wellbeing of a constantly ageing population frequently reporting with memory impairments. The project, although not directly addressing age-related memory changes is generally concerned with strategies to improve memory, a topic that can be expected to attract the interest of this broad audience, and clearly fits within the "Lifelong Health and Wellbeing" priority area of the UK research councils. The findings from this project will therefore be disseminated to the general public (see 'Pathways to Impact'), providing accessible information about mnemonic strategies and specifically about how retrieval-mediated learning can protect newly learned information against forgetting.

Fourth, the project is expected to have a significant impact on the postdoctoral researcher's and the PI's scientific work. The PI is an early career scientist who began her first permanent academic position at the University of Birmingham in autumn 2013. The project is thus expected to establish important pathways to impact for the PI's future scientific work, with the objective to initiate novel research networks with scientists in related areas, setting the stage for future collaborative projects (e.g. together with researchers in applied fields like educational psychology). The post-doctoral research assistant (PDRA) will be involved in a wide range of academic and impact activities, providing extensive scientific and methodological training and improvement of the PDRA's communication skills.
 
Description (a) In a series of now five behavioural experiments, we found evidence that active retrieval (as opposed to more passive re-exposure) does not produce the same memory benefit for visual memories as for verbal memories, and only enhances memories to the degree that the information is semantically meaningful. We additionally find that retrieval strengthens the semantic features of a visual memory relatively more than its perceptual features, consistent with a consolidation account. The findings, however, do so far not support the hypothesis that this retrieval mechanism is a fast-acting one, since all effects we observe evolve slowly, across several days. The corresponding manuscript is currently in the write-up stage.

(b) In a functional magnetic resonance imaging (fMRI) study spread over 2 days, we isolated the brain patterns related to individual or categorical memories, and then tracked how repeated recall changes the neural representation of these memories. We found evidence for our original hypothesis that rehearsing memories via retrieval, as opposed to restudy, changes the neural substrate of these memories in a way consistent with consolidation: repeated retrieval creates a neural memory trace that is more semantic-categorical in nature than the one created by restudy. Surprisingly, this "semanticization" does not come at the expense of event-unique information, which is also strengthened by retrieval. While consistent with a consolidation mechanism, the results are (like the behavioural findings described above) not supportive of a fast-acting mechanism, since all neural effects evolved slowly across days. The corresponding manuscript has been made openly available on bioRxiv, and was published in the peer-reviewed journal NeuroImage in 2019 (see publications).

(c) The overall theoretical framework for this project was published as an Opinions article in the leading journal Trends in Cognitive Sciences in 2017, and has received a high number of citations since (approx. 40). In this article, we explain why retrieval practice has specific advantages for the long-term retention of memories, beyond other rehearsal strategies, from both a neurocognitive perspective.

(d) The theoretical idea that retrieval boosts consolidation inspired another behavioural experiment, conducted by Julia Lifanov, PhD student in Dr Wimber's group. This study used a novel reaction time method to measure qualitative changes in memories over time, and found strong evidence for a "semanticization" of memories with repeated retrieval and consolidation. This study is available as preprint (Lifanov et al, 2020, bioRxiv), and was recently accepted for publication in the prestigious journal Nature Communications.
Exploitation Route The findings in (a) and (b) are highly relevant for researchers in the field. The data have been presented at various international conferences and oral presentations over the past 3 years. The PDR on this grant, Dr Catarina Ferreira, has won a British Academy Fellowship that directly builds on the research conducted in this award (see "Further Funding" section), studying further how pre-existing semantic relationships will influence memory plasticity.

The data from (a) specifically are also highly relevant for practitioners in the educational sector, where the findings can inform the optimisation of learning strategies. In particular, it is important to inform students and teachers about the power of retrieval-mediated learning, compared with other study techniques. Our findings, however, also describe the limitations of the testing effect especially for visual materials, and can be directly translated into educational practice. The first publication resulting from this award (Antony et al., 2017) has already been cited 39 times, including in articles in applied journals and book chapters that give recommendations for implementing retrieval practice as a learning and long-term retention strategy in the educational sector.
Sectors Digital/Communication/Information Technologies (including Software),Education,Healthcare

 
Description British Academy Fellowhsip
Amount £316,053 (GBP)
Funding ID PF2\180009 
Organisation The British Academy 
Sector Academic/University
Country United Kingdom
Start 09/2018 
End 09/2021
 
Title Dataset for visual testing effect paper 
Description Dataset from 4 experiments investigating the testing effect in visual materials, with or without meaning. Linked to preprint "The testing effect for visual materials depends on pre-existing knowledge", DOI 10.31234/osf.io/t6jdn 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact Only recently shared with other researchers, paper still under revision, thus awaiting concrete outcomes. 
URL https://osf.io/6zf3t/
 
Description Computational model of retrieval-mediated learning 
Organisation University of California, Davis
Country United States 
Sector Academic/University 
PI Contribution Together with Dr Catarina Ferreira, former postdoctoral research on this award, we established a collaboration with Dr Anna Schapiro, University of Pennsylvania, and with Dr James W. Antony, UC Davis. The aim of the collaboration is to translate our findings, and the theoretical framework outlined in the grant proposal and in our opinions framework paper (Antony, Ferreira, Norman & Wimber, 2018, Trends in Cognitive Sciences), into a formal computational model of retrieval-mediated learning.
Collaborator Contribution Dr Ferreira will lead on this collaboration, with myself as the senior researcher. Dr Schapiro and Dr Antony will provide their expertise in computational modeling.
Impact This is a multi-disciplinary collaboration between cognitive neuroscientists and computational modellers.
Start Year 2021
 
Description Computational model of retrieval-mediated learning 
Organisation University of Pennsylvania
Country United States 
Sector Academic/University 
PI Contribution Together with Dr Catarina Ferreira, former postdoctoral research on this award, we established a collaboration with Dr Anna Schapiro, University of Pennsylvania, and with Dr James W. Antony, UC Davis. The aim of the collaboration is to translate our findings, and the theoretical framework outlined in the grant proposal and in our opinions framework paper (Antony, Ferreira, Norman & Wimber, 2018, Trends in Cognitive Sciences), into a formal computational model of retrieval-mediated learning.
Collaborator Contribution Dr Ferreira will lead on this collaboration, with myself as the senior researcher. Dr Schapiro and Dr Antony will provide their expertise in computational modeling.
Impact This is a multi-disciplinary collaboration between cognitive neuroscientists and computational modellers.
Start Year 2021
 
Description Opinions paper outlining new memory framework with researchers at Princeton University (US) 
Organisation Princeton University
Department Department of Psychology
Country United States 
Sector Academic/University 
PI Contribution The collaboration was initiated at the International Conference on Memory (2016, Budapest, Hungary), where Dr Catarina S. Ferreira, postdoctoral member of the research team, presented project data on a poster. We were approached by Dr James Antony and Prof Kenneth Norman, who found that the basic working theory of our project (i.e., the research award "Retrieval as a fast route to memory consolidation") strongly overlapped with their own ideas of how memories are transformed over time. We decided to formalise the ideas and submit as an opinions paper to a high ranking journal in the field. As a PI, my contribution to this collaboration is the very basic idea that retrieval acts as a fast route to consolidation, as proposed in the ESRC research grant. My postdoctoral researcher Catarina Ferreira contributed human brain imaging data to the project. Together, Catarina Ferreira and I contributed to the writing of the manuscript.
Collaborator Contribution Our collaborators in Princeton contributed to formalising the framework (from a computational perspective), performed additional literature research regarding memory consolidation, to and to writing the manuscript.
Impact Research manuscript under review: Antony JW, Ferreira CS, Norman KA, Wimber MW (under review). Retrieval as a fast route to memory consolidation. Trends in Cognitive Neurosciences.
Start Year 2016
 
Description BBC Reel 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Former PI on the award, Dr Maria Wimber, was interviewed by the BBC regarding her work on memory retrieval, the human brain, and the reconstructive nature of our memories.
Year(s) Of Engagement Activity 2020
URL https://www.bbc.com/reel/video/p095rkvg/can-you-really-have-a-photographic-memory-
 
Description BBC World Service Radio Interview 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Interview with BBC World Services about our publication "Feature-specific reaction times reveal a semanticisation of memories over time and with repeated remembering", and memory and learning strategies more generally. Featuring Maria Wimber as principal investigator of the project.
Year(s) Of Engagement Activity 2021
URL https://www.bbc.co.uk/sounds/play/w172xzl6l2mw72f
 
Description Girls do Science 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Team member Catarina Ferreira gave a presentation followed by discussion for an event called "Girls do Science". This is a satellite event of Pint of Science, aimed at 12-18 year olds, where they can engage with scientists and ask questions. This is aimed at sparking their interest in science, and show them female role models.
Year(s) Of Engagement Activity 2018
URL https://pintofscience.co.uk/event/girls-do-science
 
Description Open day memory talk 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Principal investigator gave an open lecture about memory and memory disorders at the University of Birmingham's Open Day in Oct 2018. This is open to the general public, but maily aimed at future students and their parents. There were plenty of questions and a vivid discussion after the talk.
Year(s) Of Engagement Activity 2018
 
Description Pint of Science May 2019 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Postdoctoral researcher on this project, Dr Catarina Ferreira, took part in a public engagement activity as part of Pint of Science (May 2019) where visitors to the stall could learn about the brain and build models of neurons.
Year(s) Of Engagement Activity 2019
URL https://pintofscience.co.uk/
 
Description Press interviews 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Maria Wimber organised a symposium entitled the "Neurobiology of Forgetting" at the Annual Meeting of the Society for Neuroscience, the largest neuroscience meeting worldwide. In this symposium she presented the results of the fMRI study conducted within this research award. Several journalists became interested and asked for interviews afterwards. To my knowledge, these interviews resulted in at least two online media articles:
https://www.knowablemagazine.org/article/mind/2019/why-we-forget
https://www.newscientist.com/article/2187699-brain-scans-reveal-why-your-brain-forgets-details/
Year(s) Of Engagement Activity 2018
URL https://www.knowablemagazine.org/article/mind/2019/why-we-forget