Produção Nacional
Revisado por pares
Active memory reactivation previous to the introduction of a new related content improves students’ learning
2018; American Physical Society; Volume: 42; Issue: 1 Linguagem: Inglês
10.1152/advan.00077.2017
ISSN1522-1229
AutoresPriscila Marques Sosa, Rithiele Gonçalves, Felipe P. Carpes, Pâmela Billig Mello‐Carpes,
Tópico(s)Science Education and Pedagogy
ResumoIlluminationsActive memory reactivation previous to the introduction of a new related content improves students' learningPriscila Marques Sosa, Rithiele Gonçalves, Felipe P. Carpes, and Pâmela B. Mello-CarpesPriscila Marques SosaPhysiology Research Group, Federal University of Pampa, Uruguaiana, Rio Grande do Sul, Brazil, Rithiele GonçalvesPhysiology Research Group, Federal University of Pampa, Uruguaiana, Rio Grande do Sul, Brazil, Felipe P. CarpesApplied Neuromechanics Research Group, Federal University of Pampa, Uruguaiana, Rio Grande do Sul, Brazil, and Pâmela B. Mello-CarpesPhysiology Research Group, Federal University of Pampa, Uruguaiana, Rio Grande do Sul, BrazilPublished Online:04 Jan 2018https://doi.org/10.1152/advan.00077.2017MoreSectionsPDF (115 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat INTRODUCTIONTeaching-learning processes need to be constantly revised to interest and engage students in the classroom (18). In recent years, the volume of information accessible to the students has increased, and it has become a challenge to the teaching-learning process to turn classrooms into a place of active student participation (4).The wide range of content delivered by different courses, and the variety of topics addressed in these courses, make it difficult for students to retain information (9). Among health professions, for example, students learn anatomy, histology, biochemistry, physiology, kinesiology, and other life science topics, and they need not only to recall the content, but also to integrate it into new information (2). Therefore, strategies that help students retain information may be useful in promoting learning (2).Learning involves memory formation, a process that follows the steps of acquisition, consolidation, and recall (8). Acquisition represents the moment of learning. Consolidation represents the formation of a long-term memory. It involves gene expression and protein synthesis that modify synapses of specific brain structures, which means it requires time. During this time, we can use a temporary storage of information, i.e., short-term memory. Finally, recall represents the moment of remembering (8). Each time a memory is evoked and retrieved, the synapses where the information is stored are reactivated, become labile, and can be modified. These synapses can be strengthened or weakened by a process known as reconsolidation, which allows integration of a previous knowledge into a new one (16). There is a relationship between these memory events: reconsolidation is important to enrich and modify a memory, and retrieval (reactivation) seems to improve reconsolidation, which can be verified by latter memory recall (14, 17).In animals, memory reactivation facilitates reconsolidation and contributes to the persistence of different types of memory (14). In humans, it was recently shown that memory reactivation by retrieval significantly improved learning (17). Strategies to improve learning and memory could be applied in formal education. Several studies have shown that the influence of students' prior knowledge retrieval on learning is significant (3). However, there are few studies addressing these processes.Here we propose a way to promote memory reactivation by its retrieval before presenting new concepts in physiology and kinesiology classes. We also determine the influence of this strategy on students' academic performance. The intervention was conducted during an academic semester, and the results were compared with data from the previous semester when the activity had not been developed.The proposal characteristics.This study was implemented during the second semester of 2015. The 83 students [52 women and 31 men, aged 25 (SD 7) yr] were enrolled in the Human Physiology course of Nursing (n = 18) and Physiotherapy (n = 23) programs, and in the Kinesiology course of the Physical Education program (n = 42), at the Federal University of Pampa (Uruguaiana, Rio Grande do Sul, Brazil). The criterion for inclusion was participation in at least 80% of the tests conducted. The course was offered as one class/wk for the 17 wk of the academic semester. The Institutional Education Committee approved this proposal (Institutional Review Board no. 10.078.14), and students formally agreed in participate.In this protocol, we prompted the reactivation of a previously formed memory in every class by giving students a test, which we call "retrieval activity." This activity addressed concepts from the previous class. Students spent up to 15 min working on the retrieval activity. Other activities in the curriculum (lectures, exams, experiment reports, laboratory activities) were performed as usual in the remaining class time.Every retrieval activity was conducted as follows:In the beginning of each class, a test referring to the content from the previous class was distributed to the students. Each test included either a single open question or a sequence of multiple choices questions answered individually, without the students consulting books or notes (closed-book test). For example, before the introduction of content related to mechanisms of blood pressure control, the test question in the retrieval activity, "What are the main differences between action potentials of skeletal muscle and cardiac muscle, and what determine these differences?", was presented to the students. The answer required the retrieval of knowledge about cardiac cell characteristics and electrophysiology fundamental to the understanding of baroreceptor reflex, which was presented in previous classes.The tests were collected, shuffled, and then redistributed among the students. Professor and students discussed the correct answers and resolved questions or misconceptions. This stage was important because it allowed students to verify errors and learn from them (13). The whole process lasted up to 15 min, on average. Although the retrieval activity took up part of the class, the 15 min did not compromise the course, because, during this time, the professor also checked for the presence of the students and wrote notes on the blackboard.After the retrieval activity, the new content was introduced, and the traditional class followed with the regular activities.At the end of the semester the students answered a questionnaire including close-ended questions (Table 1) to evaluate their impressions about the proposed method. Students also were able to leave anonymous comments and suggestions about the activity.Table 1. Questions used to evaluated the retrieval activities and students' responsesResponse, %QuestionYesNoNRA. At the beginning of the semester, when the retrieval activities were proposed, were you favorable to the method?78211B. If not, did you change your mind?173845C. Did this dynamic of retrieval activities in the beginning of the classes contribute to your understanding and comprehension of the class content?9361D. Did this dynamic of retrieval activities in the beginning of the class help you to increase your frequency of study?73243E. Did this dynamic of retrieval activities in the beginning of the class help you to identify your difficulties in understanding of content?88111F. Do you have a habit of studying or revising the content of the previous class to prepare for the retrieval activities?57430G. Do you think that the retrieval activities helped to increase your learning?Results shown in Fig. 1A ( ) Yes ( ) No ( ) PartiallyH. The second stage of the dynamic proposed the correction and discussion of contents with the whole class participation. How do you classify this stage?Results shown in Fig. 1B ( ) Necessary, good ( ) Good ( ) Unnecessary ( ) Other:I. In your opinion, the degree of difficulty of the questions proposed in the retrieval activities were:Results shown in Fig. 1C ( ) Easy ( ) Normal ( ) Difficult ( ) Very difficultJ. Would you recommend including weekly retrieval activities in other courses?8515Values are in %; n = 83 students. NR, no response.To investigate whether retrieval activities resulted in improved performance in the course, the final grades of the students participating in this project were compared with the grades from students in the previous semester, when retrieval activities were not conducted. Students from the previous semester (n = 92) had classes addressing the same content and delivered by the same professors. This comparison was possible because the final grade for both semesters was determined by different tests that covered the same content. In our institution, the grades can vary from 0 to 10, and the minimal grade needed to pass the course is 6.Table 1 shows the results of the questionnaire. The results of the final exam performed in the end of semester are presented in Fig. 2 as mean (SD), and groups were compared using independent t-test with significance level of 0.05.RESULTSIn the beginning of the semester, the retrieval activity was well received by the students (Table 1, question A). As the course developed, those students who showed some concern about the proposal changed their mind to a favorable opinion (Table 1, question B).When students were asked about how the retrieval activities contributed to their comprehension of the content, we observed that 93% of the students (n = 76) replied that the retrieval activities contributed positively (Table 1, question C). Furthermore, 73% (n = 60) reported that the retrieval activities helped to increase their weekly study frequency (Table 1, question D), and 88% (n = 72) stated that the retrieval activities helped them to identify difficulties in their content understanding (Table 1, question E).More than one-half of the students (n = 47, Table 1, question F) affirmed that the retrieval activities motivated them to acquire the habit of studying or revising notes outside of class during the week. Most of students (59%; n = 48, Fig. 1A) said that the retrieval activities contributed to increasing their learning, and 35% reported that it contributed partially to increasing their learning (n = 29, Fig. 1A).Fig. 1.Students' opinion about the retrieval activities' contribution to their learning (A), the second stage of the proposal (correction and discussion of test question in a collaborative way; B), and the degree of difficulty of the tests (n = 83; C). NR, no response; V. Difficult, very difficult.Download figureDownload PowerPointThe second stage of the proposal involved the correction and discussion of test questions in collaboration with professor and colleagues. The majority of the students classified this as good or necessary, whereas 5% reported that this phase could be waived (Fig. 1B). When asked about the degree of difficulty of the tests, 69% responded that tests were of normal difficulty, 26% very difficult, and 5% considered them easy (Fig. 1C). In the last class of the semester, 85% of the students affirmed they would recommend that retrieval activities be incorporated into other courses in their academic career (Table 1, question J).We verified that the students participating in the retrieval activities achieved better grades compared with the students from the previous semester, when retrieval activities were not performed (grades: 6.99 ± 0.19) for students enrolled in retrieval activities vs. 5.89 ± 0.22 for students not enrolled in retrieval activities; P < 0.0001; Fig. 2). Additionally, in the previous semester, the mean failure rate was 27%, whereas, in the semester when retrieval activities were performed, the failure rate was 13%.Fig. 2.Comparison of end-of-semester test scores for retrieval activity students and non-retrieval activity students. ***P < 0.0001, unpaired Student's t-test (n = 83 out of 92/group). Each group of students represents a class (comparison between classes of two successive semesters). RA, students enrolled in retrieval activity; NRA, students not enrolled in retrieval activity.Download figureDownload PowerPointSignificance.Our results indicate that a formal active retrieval of previous knowledge (memory reactivation) through short tests performed before presentation of new related content can be an effective strategy to improve students' engagement with the content and can potentially contributes to the achievement of higher final grades. These results suggest that active memory reactivation by retrieval improved memory reconsolidation, and, as a consequence, improved content recall, which may have contributed to the higher grades obtained in summative tests. Additionally, based on the students' feedback, the retrieval activity influenced students' behavior by increasing the frequency of weekly study. In general, the students appreciated and recommended the implementation of this strategy in physiology, kinesiology, and other courses.In addition to utilizing dynamic strategies to increase the interest of students, it is important that professors understand the neurobiological mechanisms of learning and memory and consider implementing them in their methodological choices. Studies have shown that new memories are stabilized after an initial significant learning experience, in a process called consolidation (11). However, in daily life, another crucial process of the learning experience, memory reconsolidation, occurs because we are constantly experiencing situations related to previous learning (prior knowledge that is stored in our memory) and need to retrieve consolidated memories and to make them labile (susceptible to changes) (5).In physiology, kinesiology, and other classes, students are frequently promoting reconsolidation; for example, when they remember the anatomical or histological structures of an organ to better understand its function. In this moment, students need to retrieve prior knowledge of anatomy and histology and add new information about the function of specific organs to the already existing memory, which characterizes reconsolidation. We know that educational and cognitive neuroscience literature are not completely integrated, and that the two fields use different terminologies. Moreover, concepts may not be entirely equivalent in these areas, but our goal is to show that neuroscience laboratory and clinical experimental findings can be integrated to improve classroom practices and learning.Additional evidence supportive of this proposal can be found in a previous study of the impact of retrieval practices on memory tests (17). Participants were able to recall more items that were previously retrieved in comparison to items that were not tested or that they had restudied (17). In another study, involving medical students learning about a specific cardiac medical practice, results showed that active retrieval improved learning and retention of related content (10). One group of students practiced active retrieval by verbally identifying unlabeled cardiac anatomical structures (memory retrieval) within 10 s of viewing a video clip addressing the contents, whereas another group watched the same video, but without generating an answer (10).In education, it is clear that prior knowledge influences students' learning (3), but neuroscience shows the importance of activating previous knowledge before learning a new concept. The formal memory reactivation (retrieval) occurring before inclusion of new related information can trigger and improve the reconsolidation process (6), which in turn can result in better memory recall or learning improvement (7, 12). Furthermore, memory reactivation is important for the enhancement of the interaction between the hippocampus and neocortex, promoting memory strengthening and long-term storage (15).Based on these neurobiological concepts, we propose the use of tests to induce memory retrieval of previous knowledge related to the new topic that will be introduced in a class. This strategy should promote better learning, primarily through improved memory reconsolidation. In our study, we considered closed-book tests. However, we assume that our proposal could also be performed using an open-book format, since a previous report that compared closed-book and open-book tests found similar results in long-term retention (1).Our results showed that students' performance in a final summative exam was better when the retrieval activity (a formal active memory reactivation) was conducted. Additionally, the students classified the method as positive and reported that it helped them to better understand content, identify difficulties, and study more frequently.GRANTSP. M. Sosa was supported by a Federal University of Pampa fellow grant. P. B. Mello-Carpes was supported by a For Women in Science- L'Oreal/UNESCO fellow grant. R Gonçalves was supported by a CAPES fellow grant. F. P. Carpes was supported by a CNPq research fellow grant.DISCLOSURESNo conflicts of interest, financial or otherwise, are declared by the authors.AUTHOR CONTRIBUTIONSP.M.S., R.G., F.P.C., and P.B.M.-C. performed experiments; P.M.S., F.P.C., and P.B.M.-C. analyzed data; P.M.S., R.G., F.P.C., and P.B.M.-C. interpreted results of experiments; P.M.S., R.G., and P.B.M.-C. prepared figures; P.M.S., F.P.C., and P.B.M.-C. drafted manuscript; P.M.S., R.G., F.P.C., and P.B.M.-C. edited and revised manuscript; P.M.S., R.G., F.P.C., and P.B.M.-C. approved final version of manuscript; P.B.M.-C. conceived and designed research.REFERENCES1. Agarwal PK, Karpicke JD, Kang SHK, Roediger HL III, McDermott KB. Examining the testing effect with open- and closed-book tests. Appl Cogn Psychol 22: 861–876, 2008. doi:10.1002/acp.1391.Crossref | ISI | Google Scholar2. Bonora M, Wieckowsk MR, Chinopoulos C, Kepp O, Kroemer G, Galluzzi L, Pinton P. Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition. Oncogene 34: 1608, 2015. doi:10.1038/onc.2014.462. Crossref | PubMed | ISI | Google Scholar3. Dochy F, De Rijdt C, Dyck W. Cognitive prerequisites and learning how far have we progressed since bloom? Implications for educational practice and teaching. Active Learn High Educ 3: 265–284, 2002. doi:10.1177/1469787402003003006.Crossref | Google Scholar4. Dunlosky J, Rawson KA, Marsh EJ, Nathan MJ, Willingham DT. Improving students' learning with effective learning techniques: promising directions from cognitive and educational psychology. Psychol Sci Public Interest 14: 4–58, 2013. doi:10.1177/1529100612453266. Crossref | PubMed | ISI | Google Scholar5. Forcato C, Burgos VL, Argibay PF, Molina VA, Pedreira ME, Maldonado H. Reconsolidation of declarative memory in humans. Learn Mem 14: 295–303, 2007. doi:10.1101/lm.486107. Crossref | PubMed | ISI | Google Scholar6. Fukushima H, Zhang Y, Archbold G, Ishikawa R, Nader K, Kida S. Enhancement of fear memory by retrieval through reconsolidation. eLife 3: e02736, 2014. doi:10.7554/eLife.02736. Crossref | PubMed | ISI | Google Scholar7. Gisquet-Verrier P, Riccio DC. Memory reactivation effects independent of reconsolidation. Learn Mem 19: 401–409, 2012. doi:10.1101/lm.026054.112. Crossref | PubMed | ISI | Google Scholar8. Izquierdo I, Barros DM, Mello e Souza T, de Souza MM, Izquierdo LA, Medina JH. Mechanisms for memory types differ. Nature 393: 635–636, 1998. doi:10.1038/31371. Crossref | PubMed | ISI | Google Scholar9. Khoiriyah U, Roberts C, Jorm C, Van der Vleuten CP. Enhancing students' learning in problem based learning: validation of a self-assessment scale for active learning and critical thinking. BMC Med Educ 15: 140, 2015. doi:10.1186/s12909-015-0422-2. Crossref | PubMed | ISI | Google Scholar10. Kleiman AM, Forkin KT, Bechtel AJ, Collins SR, Ma JZ, Nemergut EC, Huffmyer JL. Generative retrieval improves learning and retention of cardiac anatomy using transesophageal echocardiography. Anesth Analg 124: 1440–1444, 2017. doi:10.1213/ANE.0000000000002004. Crossref | PubMed | ISI | Google Scholar11. McGaugh JL. Memory—a century of consolidation. Science 287: 248–251, 2000. doi:10.1126/science.287.5451.248. Crossref | PubMed | ISI | Google Scholar12. Merlo E, Ratano P, Ilioi EC, Robbins MA, Everitt BJ, Milton AL. Amygdala dopamine receptors are required for the destabilization of a reconsolidating appetitive memory. eNeuro 2: 1–14, 2015. doi:10.1523/ENEURO.0024-14.2015. Crossref | PubMed | ISI | Google Scholar13. Metcalfe J. Learning from errors. Annu Rev Psychol 68: 465–489, 2017. doi:10.1146/annurev-psych-010416-044022. Crossref | PubMed | ISI | Google Scholar14. Rossato JI, Bevilaqua LR, Medina JH, Izquierdo I, Cammarota M. Retrieval induces hippocampal-dependent reconsolidation of spatial memory. Learn Mem 13: 431–440, 2006. doi:10.1101/lm.315206. Crossref | PubMed | ISI | Google Scholar15. Schlichting ML, Preston AR. Memory reactivation during rest supports upcoming learning of related content. Proc Natl Acad Sci USA 111: 15845–15850, 2014. doi:10.1073/pnas.1404396111. Crossref | PubMed | ISI | Google Scholar16. Schwabe L, Nader K, Pruessner JC. Reconsolidation of human memory: brain mechanisms and clinical relevance. Biol Psychiatry 76: 274–280, 2014. doi:10.1016/j.biopsych.2014.03.008. Crossref | PubMed | ISI | Google Scholar17. Sutterer DW, Awh E. Retrieval practice enhances the accessibility but not the quality of memory. Psychon Bull Rev 23: 831–841, 2016. doi:10.3758/s13423-015-0937-x. Crossref | PubMed | ISI | Google Scholar18. Zhang Q, Lee L, Gruppen LD, Ba D. Medical education: changes and perspectives. Med Teach 35: 621–627, 2013. doi:10.3109/0142159X.2013.789495. Crossref | PubMed | ISI | Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: P. Mello-Carpes. Physiology Research Group, Stress, Memory and Behavior Lab, Federal University of Pampa, BR 472, Km 592, PO Box 118, Uruguaiana, RS 97500-970, Brazil (e-mail: [email protected]edu.br). Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Collections Cited ByEffect of an active learning methodology combined with formative assessments on performance, test anxiety, and stress of university studentsLais Tono Cardozo, Maria Antonia Ramos de Azevedo, Maeline Santos Morais Carvalho, Rafaela Costa, Patricia Oliveira de Lima, and Fernanda Klein Marcondes18 November 2020 | Advances in Physiology Education, Vol. 44, No. 4Use of Facebook groups as a strategy for continuum involvement of students with physiology after finishing a physiology coursePriscila Marques Sosa,* Guilherme Salgado Carrazoni,* Rithiele Gonçalves, and Pâmela Billig Mello-Carpes22 June 2020 | Advances in Physiology Education, Vol. 44, No. 3Integrating synapse, muscle contraction, and autonomic nervous system game: effect on learning and evaluation of students' opinionsLais Tono Cardozo,* Amicio Pina Castro,* Alexsandro Ferreira Guimarães, Lucila Ludmila Paula Gutierrez, Luís Henrique Montrezor, and Fernanda Klein Marcondes13 March 2020 | Advances in Physiology Education, Vol. 44, No. 2Anatomical Sciences Education, Vol. 13, No. 2Teaching Operations Planning at the Undergraduate Level6 June 2019 | SAGE Open, Vol. 9, No. 2 More from this issue > Volume 42Issue 1March 2018Pages 75-78 Copyright & PermissionsCopyright © 2018 the American Physiological Societyhttps://doi.org/10.1152/advan.00077.2017PubMed29341807History Received 1 June 2017 Accepted 29 November 2017 Published online 4 January 2018 Published in print 1 March 2018 Metrics
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