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The rodent object-in-context task: A systematic review and meta-analysis of important variables

Sep, Milou S. C., Vellinga, Marijn, Sarabdjitsingh, R. Angela, Joëls, Marian·2021·PLOS ONE
DOI 10.1371/journal.pone.0249102PMC PMC8284613
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Abstract

Environmental information plays an important role in remembering events. Information about stable aspects of the environment (here referred to as ‘context’) and the event are combined by the hippocampal system and stored as context-dependent memory. In rodents (such as rats and mice), context-dependent memory is often investigated with the object-in-context task. However, the implementation and interpretation of this task varies considerably across studies. This variation hampers the comparison between studies and—for those who design a new experiment or carry out pilot experiments–the estimation of whether observed behavior is within the expected range. Also, it is currently unclear which of the variables critically influence the outcome of the task. To address these issues, we carried out a preregistered systematic review (PROSPERO CRD42020191340) and provide an up-to-date overview of the animal-, task-, and protocol-related variations in the object-in-context task for rodents. Using a data-driven explorative meta-analysis we next identified critical factors influencing the outcome of this task, such as sex, testbox size and the delay between the learning trials. Based on these observations we provide recommendations on sex, strain, prior arousal, context (size, walls, shape, etc.) and timing (habituation, learning, and memory phase) to create more consensus in the set-up, procedure, and interpretation of the object-in-context task for rodents. This could contribute to a more robust and evidence-based design in future animal experiments.

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Figures

Fig 1 Schematic overview of the rodent object-in-context task (OIC). During the sample phase (learning) an animal encounters a unique set of two objects in context A and next a different set in B. In the test phase (memory) the animal is exposed to either context A or B, with one object of each unique set.
Fig 1 Schematic overview of the rodent object-in-context task (OIC). During the sample phase (learning) an animal encounters a unique set of two objects in context A and next a different set in B. In the test phase (memory) the animal is exposed to either context A or B, with one object of each unique set.CC BY · PubMed Central
Fig 2 Flowchart of the study.
Fig 2 Flowchart of the study.CC BY · PubMed Central
Fig 3 Assessment of study quality (QA) and risk of bias. The risk of bias according to SYRCLE’s risk of bias (RoB) tool [34], for each study, indicated by PubMed ID (PMID), included in the systematic review. The figure also shows if an a priori sample size calculation was performed and -if behavior was scored manually- an inter-observer rate was calculated. Unreported details were scored as an ‘unclear’ risk of bias.
Fig 3 Assessment of study quality (QA) and risk of bias. The risk of bias according to SYRCLE’s risk of bias (RoB) tool [34], for each study, indicated by PubMed ID (PMID), included in the systematic review. The figure also shows if an a priori sample size calculation was performed and -if behavior was scored manually- an inter-observer rate was calculated. Unreported details were scored as an ‘unclear’ risk of bias.CC BY · PubMed Central
Fig 4 Forest plot. Forest plot visualizing the Discrimination Ratio (DR) per experimental group, per study; and the overall mean DR with 95% Confidence Interval. Studies are presented by publication year in ascending order.
Fig 4 Forest plot. Forest plot visualizing the Discrimination Ratio (DR) per experimental group, per study; and the overall mean DR with 95% Confidence Interval. Studies are presented by publication year in ascending order.CC BY · PubMed Central
Fig 5 Funnel plot. Funnel plot showing the DR of individual control groups on the x-axis against their standard errors (i.e., the square root of the sampling variances) on the y-axis. Vertical reference lines indicate the 0, i.e. no context-dependent memory; and the estimated overall mean DR based on the model. Colors indicate unique studies (PMID).
Fig 5 Funnel plot. Funnel plot showing the DR of individual control groups on the x-axis against their standard errors (i.e., the square root of the sampling variances) on the y-axis. Vertical reference lines indicate the 0, i.e. no context-dependent memory; and the estimated overall mean DR based on the model. Colors indicate unique studies (PMID).CC BY · PubMed Central
Fig 6 Relative importance of potential moderators based on ‘permuted variable importance’ in the random forest-based meta-analyses. Moderators above the horizontal line belong to the top 50%. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively.
Fig 6 Relative importance of potential moderators based on ‘permuted variable importance’ in the random forest-based meta-analyses. Moderators above the horizontal line belong to the top 50%. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively.CC BY · PubMed Central
Fig 7 Partial dependence plots showing the predicted relation between DR and the upper half most important variables in the random forest-based meta-analysis, broken down by species: Mice in red vs. rat in blue. The y-axis shows the predicted DR and x-axis shows the values of the variable that is named above the graph (in gray). The values of context.size A and B are shown in in cm2 and the values of time variables (learning. learning.delay, learning.time.trial, habituation.time.total.context, habituation.time.trial) are shown in minutes. Higher context.difference.score values indicate more different contexts and higher arousal.prior values indicate more arousal prior to the experiment. Strains values are abbreviations: TMm (Tg(Sim1cre)KH21Gsat/Mmucd mice), SEm (SEm Sv/Ev mice), ICm (ICR mice), BLm (C57BL/6 mice), LHr (Lister hooded rats), LEr (Long-Evans rats), SDr (Sprague-Dawley rats), Wr (Wistar rats), pDr (pigmented DA strain rats), DAr (Dark Agouti rats). DR.formula values are also abbreviations: n-f/t ((Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)), n-f/t*100 ([(Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)]*100), n/t ((Tnovel)/(Tnovel+Tfamiliar)), n/t*100 ([(Tnovel)/(Tnovel+Tfamiliar)]*100). The context.order value AA indicates that memory was tested in the context of the second learning trial, the value AB indicates that memory was tested in the context of the first learning trial, ‘both’ indicates that AA and AB were randomized. Finally, context.habituation.freq values show the number of visits per context. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively. Note, predictions based on the random forest-model do not take into account that strains belong to a specific species (either rat or mouse), hence rat and mice predictions were generated of all strains.
Fig 7 Partial dependence plots showing the predicted relation between DR and the upper half most important variables in the random forest-based meta-analysis, broken down by species: Mice in red vs. rat in blue. The y-axis shows the predicted DR and x-axis shows the values of the variable that is named above the graph (in gray). The values of context.size A and B are shown in in cm2 and the values of time variables (learning. learning.delay, learning.time.trial, habituation.time.total.context, habituation.time.trial) are shown in minutes. Higher context.difference.score values indicate more different contexts and higher arousal.prior values indicate more arousal prior to the experiment. Strains values are abbreviations: TMm (Tg(Sim1cre)KH21Gsat/Mmucd mice), SEm (SEm Sv/Ev mice), ICm (ICR mice), BLm (C57BL/6 mice), LHr (Lister hooded rats), LEr (Long-Evans rats), SDr (Sprague-Dawley rats), Wr (Wistar rats), pDr (pigmented DA strain rats), DAr (Dark Agouti rats). DR.formula values are also abbreviations: n-f/t ((Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)), n-f/t*100 ([(Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)]*100), n/t ((Tnovel)/(Tnovel+Tfamiliar)), n/t*100 ([(Tnovel)/(Tnovel+Tfamiliar)]*100). The context.order value AA indicates that memory was tested in the context of the second learning trial, the value AB indicates that memory was tested in the context of the first learning trial, ‘both’ indicates that AA and AB were randomized. Finally, context.habituation.freq values show the number of visits per context. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively. Note, predictions based on the random forest-model do not take into account that strains belong to a specific species (either rat or mouse), hence rat and mice predictions were generated of all strains.CC BY · PubMed Central
Fig 8 Weighted scatter plots showing the distribution of the raw DR for the 50% most important variables in the random forest-based meta-analysis, broken down by species: Mice in red vs. rat in blue. Dot size indicates the sample size of each observation. Most studies were performed in rats. The y-axis shows the mean DR and x-axis shows the values of the variable that is named below the graph. The values of context.size A and B are shown in in cm2 and the values of time variables (learning. learning.delay, learning.time.trial, habituation.time.total.context, habituation.time.trial) are shown in minutes. Higher context.difference.score values indicate more different contexts and higher arousal.prior values indicate more arousal prior to the experiment. Strains values are abbreviations: TMm (Tg(Sim1cre)KH21Gsat/Mmucd mice), SEm (SEm Sv/Ev mice), ICm (ICR mice), BLm (C57BL/6 mice), LHr (Lister hooded rats), LEr (Long-Evans rats), SDr (Sprague-Dawley rats), Wr (Wistar rats), pDr (pigmented DA strain rats), DAr (Dark Agouti rats). DR.formula values are also abbreviations: n-f/t ((Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)), n-f/t*100 ([(Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)]*100), n/t ((Tnovel)/(Tnovel+Tfamiliar)), n/t*100 ([(Tnovel)/(Tnovel+Tfamiliar)]*100). The context.order value AA indicates that memory was tested in the context of the second learning trial, the value AB indicates that memory was tested in the context of the first learning trial, ‘both’ indicates that AA and AB were randomized. Finally, context.habituation.freq values show the number of visits per context. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively.
Fig 8 Weighted scatter plots showing the distribution of the raw DR for the 50% most important variables in the random forest-based meta-analysis, broken down by species: Mice in red vs. rat in blue. Dot size indicates the sample size of each observation. Most studies were performed in rats. The y-axis shows the mean DR and x-axis shows the values of the variable that is named below the graph. The values of context.size A and B are shown in in cm2 and the values of time variables (learning. learning.delay, learning.time.trial, habituation.time.total.context, habituation.time.trial) are shown in minutes. Higher context.difference.score values indicate more different contexts and higher arousal.prior values indicate more arousal prior to the experiment. Strains values are abbreviations: TMm (Tg(Sim1cre)KH21Gsat/Mmucd mice), SEm (SEm Sv/Ev mice), ICm (ICR mice), BLm (C57BL/6 mice), LHr (Lister hooded rats), LEr (Long-Evans rats), SDr (Sprague-Dawley rats), Wr (Wistar rats), pDr (pigmented DA strain rats), DAr (Dark Agouti rats). DR.formula values are also abbreviations: n-f/t ((Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)), n-f/t*100 ([(Tnovel-Tfamiliar)/(Tnovel+Tfamiliar)]*100), n/t ((Tnovel)/(Tnovel+Tfamiliar)), n/t*100 ([(Tnovel)/(Tnovel+Tfamiliar)]*100). The context.order value AA indicates that memory was tested in the context of the second learning trial, the value AB indicates that memory was tested in the context of the first learning trial, ‘both’ indicates that AA and AB were randomized. Finally, context.habituation.freq values show the number of visits per context. Full definitions of variables and sum scores can be found in A2 and A5 Appendices in S1 File respectively.CC BY · PubMed Central

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Metadata

Authors
Sep, M. S. C., Vellinga, M., Sarabdjitsingh, R. A., & Joëls, M.
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2021-07-16
Volume
16
Issue
7
Pages
e0249102
ISSN
1932-6203
DOI
10.1371/journal.pone.0249102
PMC
PMC8284613
Cited by
17
References
13
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • ZonMw (114024150)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (022.003.003)
  • ministerie van defensie
  • Ministerie van Onderwijs, Cultuur en Wetenschap (024.001.003)

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