Combining Animal Welfare With Experimental Rigor to Improve Reproducibility in Behavioral Neuroscience.
Open accessAbstract
Grants of Alexander von Humboldt Foundation (Germany) to CLi. CML was recipient of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) research fellowship through the Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (INCT-TM), Brazil. FM was supported by Post-doctoral fellowship grant #2018/25857-5, São Paulo Research Foundation (FAPESP), Brazil. KD was supported by Fellow BIPD/FCT Proj2020/i3S/26040705/2021, Fundação para a Ciência e Tecnologia, Portugal. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Positive welfare manipulations may contribute to improved model validity and data reproducibility.
“The use of manipulations to enhance positive welfare in laboratory animals has been shown not to be a source of variability ( Kentner et al., 2021), and a possible contribution towards improved model validity and data reproducibility ( Loss et al., 2021; Van De Weerd et al., 2004; Würbel & Garner, 2007).”
From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Loss et al., 2021
The use of manipulations to enhance positive welfare in laboratory animals has been shown not to be a source of variability.
“The use of manipulations to enhance positive welfare in laboratory animals has been shown not to be a source of variability ( Kentner et al., 2021), and a possible contribution towards improved model validity and data reproducibility ( Loss et al., 2021; Van De Weerd et al., 2004; Würbel & Garner, 2007).”
From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Loss et al., 2021
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Why Most Published Research Findings Are False
Ioannidis, J. P. A. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020124 · Cited by 10,505 · see citing works
Estimating the reproducibility of psychological science
Open Science Collaboration (2015) · Science · doi:10.1126/science.aac4716 · Cited by 8,515 · cited 2× · see citing works
“…“reproducibility crisis” has led to the establishment of crowdsourced initiatives around the world addressing reproducibility issues in sciences, such as behavioral neuroscience (Open Science, 2015; Freedman et al., 2017; Reproducibility Project and Cancer Biology, 2017; Amaral et al., 2019).”
BackgroundThe Structure of Scientific Revolutions
Hall, M. B., & Kuhn, T. S. (1963) · The American Historical Review · doi:10.2307/1847040 · Cited by 7,753 · see citing works
Power failure: why small sample size undermines the reliability of neuroscience
Button, K. S., Ioannidis, J. P. A., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S. J., & Munafò, M. R. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3475 · Cited by 7,641 · cited 1× · see citing works
“The lack of a rigorous plan results in the massive production of underpowered exploratory studies (Maxwell, 2004; Button et al., 2013; Lazic, 2018), with the aggravating factor that they are often misinterpreted as confirmatory studies ones (Wagenmakers et al.”
BackgroundSYRCLE’s risk of bias tool for animal studies
Hooijmans, C. R., Rovers, M. M., de Vries, R. B., Leenaars, M., Ritskes-Hoitinga, M., & Langendam, M. W. (2014) · BMC Medical Research Methodology · doi:10.1186/1471-2288-14-43 · Cited by 4,415 · see citing works
The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research
du Sert, N. P., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., et al. (2020) · Experimental Physiology · doi:10.1113/ep088870 · Cited by 3,538 · see citing works
Raise standards for preclinical cancer research
Begley, C. G., & Ellis, L. M. (2012) · Nature · doi:10.1038/483531a · Cited by 2,979 · cited 2× · see citing works
“The currently available empirical estimates on the topic suggest that less than half (ranging from 49% down to 11%) of scientific results are reproducible (Prinz et al., 2011; Begley and Ellis, 2012; Freedman et al., 2015, 2017).”
BackgroundAnimal models of neuropsychiatric disorders
Nestler, E. J., & Hyman, S. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2647 · Cited by 2,023 · see citing works
The preregistration revolution
Nosek, B. A., Ebersole, C. R., DeHaven, A. C., & Mellor, D. T. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1708274114 · Cited by 1,998 · see citing works
Believe it or not: how much can we rely on published data on potential drug targets?
Prinz, F., Schlange, T., & Asadullah, K. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3439-c1 · Cited by 1,888 · see citing works
Enriched environments, experience-dependent plasticity and disorders of the nervous system
Nithianantharajah, J., & Hannan, A. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1970 · Cited by 1,771 · see citing works
The behaviour and ecology of the zebrafish, Danio rerio
Spence, R., Gerlach, G., Lawrence, C., & Smith, C. (2007) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2007.00030.x · Cited by 1,130 · see citing works
The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research
du Sert, N. P., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., et al. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15193 · Cited by 1,121 · see citing works
Guidelines for the Design and Statistical Analysis of Experiments Using Laboratory Animals
Festing, M. F. W., & Altman, D. G. (2002) · ILAR Journal · doi:10.1093/ilar.43.4.244 · Cited by 1,110 · see citing works
The economics of reproducibility in preclinical research
Freedman, L. P., Cockburn, I. M., & Simcoe, T. S. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002165 · Cited by 1,055 · see citing works
An Agenda for Purely Confirmatory Research
Wagenmakers, E.-J., Wetzels, R., Borsboom, D., van der Maas, H. L. J., & Kievit, R. A. (2012) · Perspectives on Psychological Science · doi:10.1177/1745691612463078 · Cited by 1,042 · see citing works
Biomedical research: increasing value, reducing waste.
Macleod, M. R., Michie, S., Roberts, I., Dirnagl, U., Chalmers, I., Ioannidis, J. P. A., Salman, R. A.-S., Chan, A.-W., & Glasziou, P. (2014) · The Lancet · doi:10.1016/s0140-6736(13)62329-6 · Cited by 1,003 · see citing works
The scandal of poor medical research.
Altman, D. G. (1994) · BMJ · doi:10.1136/bmj.308.6924.283 · Cited by 897 · see citing works
Kilkenny, C., Parsons, N., Kadyszewski, E., Festing, M. F. W., Cuthill, I. C., Fry, D., Hutton, J., & Altman, D. G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007824 · Cited by 860 · see citing works
The fickle P value generates irreproducible results
Halsey, L. G., Curran‐Everett, D., Vowler, S. L., & Drummond, G. B. (2015) · Nature Methods · doi:10.1038/nmeth.3288 · Cited by 753 · see citing works
A dirty dozen: twelve p-value misconceptions.
Goodman, S. (2008) · Seminars in hematology (Print) · doi:10.1053/j.seminhematol.2008.04.003 · Cited by 694 · see citing works
Can, A., Dao, D. T., Terrillion, C. E., Piantadosi, S. C., Bhat, S., & Gould, T. D. (2011) · Journal of Visualized Experiments · doi:10.3791/3769 · Cited by 657 · see citing works
Maxwell, S. E. (2004) · Psychological Methods · doi:10.1037/1082-989x.9.2.147 · Cited by 655 · see citing works
Zebrafish in The Wild: A Review of Natural History And New Notes from The Field
Engeszer, R. E., Patterson, L. B., Rao, A. A., & Parichy, D. M. (2007) · Zebrafish · doi:10.1089/zeb.2006.9997 · Cited by 612 · see citing works
Publication bias in reports of animal stroke studies leads to major overstatement of efficacy
Sena, E. S., van der Worp, H. B., Bath, P. M. W., Howells, D. W., & Macleod, M. R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000344 · Cited by 600 · see citing works
PREPARE: guidelines for planning animal research and testing
Smith, A. J., Clutton, R. E., Lilley, E. J., Hansen, K. E. A., & Brattelid, T. (2017) · Laboratory Animals · doi:10.1177/0023677217724823 · Cited by 600 · see citing works
Mice Lacking Dopamine D4 Receptors Are Supersensitive to Ethanol, Cocaine, and Methamphetamine
Rubinstein, M., Phillips, T. J., Bunzow, J. R., Falzone, T. L., Dziewczapolski, G., Zhang, G., Fang, Y., Larson, J. L., McDougall, J. A., Chester, J. A., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)80365-7 · Cited by 473 · see citing works
Cumming, G. (2008) · Perspectives on Psychological Science · doi:10.1111/j.1745-6924.2008.00079.x · Cited by 451 · see citing works
Reproducibility of animal research in light of biological variation
Voelkl, B., Altman, N., Forsman, A., Forstmeier, W., Gurevitch, J., Jarić, I., Karp, N. A., Kas, M. J., Schielzeth, H., de Casteele, T. V., et al. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0313-3 · Cited by 391 · see citing works
The problem of pseudoreplication in neuroscientific studies: is it affecting your analysis?
Lazic, S. E. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-5 · Cited by 381 · see citing works
A practical solution to pseudoreplication bias in single-cell studies
Zimmerman, K. D., Espeland, M. A., & Langefeld, C. D. (2021) · Nature Communications · doi:10.1038/s41467-021-21038-1 · Cited by 362 · see citing works
Risk of bias in reports of in vivo research: a focus for improvement
Macleod, M. R., Lawson McLean, A., Kyriakopoulou, A., Serghiou, S., de Wilde, A., Sherratt, N., Hirst, T., Hemblade, R., Bahor, Z., Nunes-Fonseca, C., et al. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002273 · Cited by 358 · see citing works
Willner, P. (1986) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(86)90051-5 · Cited by 347 · see citing works
Halsey, L. (2019) · Biology Letters · doi:10.1098/rsbl.2019.0174 · Cited by 327 · see citing works
Baker, D., Lidster, K., Sottomayor, A., & Amor, S. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001756 · Cited by 305 · see citing works
What exactly is ‘N’ in cell culture and animal experiments?
Lazic, S. E., Clarke-Williams, C. J., & Munafò, M. R. (2018) · PLOS Biology · doi:10.1371/journal.pbio.2005282 · Cited by 291 · see citing works
Happy animals make good science.
Poole, T. (1997) · Laboratory Animals · doi:10.1258/002367797780600198 · Cited by 288 · see citing works
Models and fictions in science
Godfrey‐Smith, P. (2008) · Philosophical Studies · doi:10.1007/s11098-008-9313-2 · Cited by 252 · see citing works
van der Staay, F. J. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.01.006 · Cited by 249 · see citing works
Meijer, J. H., & Robbers, Y. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.0210 · Cited by 248 · see citing works
Lazic, S. E., & Essioux, L. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-37 · Cited by 247 · see citing works
Cage enrichment and mouse behaviour
Wolfer, D. P., Litvin, O. I., Morf, S., Nitsch, R. M., Lipp, H., & Würbel, H. (2004) · Nature · doi:10.1038/432821a · Cited by 245 · see citing works
Big data from small data: data-sharing in the 'long tail' of neuroscience
Ferguson, A. R., Nielson, J. L., Cragin, M. H., Bandrowski, A. E., & Martone, M. E. (2014) · Nature Neuroscience · doi:10.1038/nn.3838 · Cited by 211 · see citing works
Advancing biology through a deeper understanding of zebrafish ecology and evolution.
Parichy, D. M. (2015) · eLife · doi:10.7554/elife.05635 · Cited by 203 · see citing works
Lazic, S. E., & Essioux, L. (2016) · Cited by 182 · see citing works
on behalf of the IICARus Collaboration, Hair, K., Macleod, M. R., & Sena, E. S. (2019) · Research Integrity and Peer Review · doi:10.1186/s41073-019-0069-3 · Cited by 174 · see citing works
Behavioral profile of wild mice in the elevated plus-maze test for anxiety
Holmes, A., Parmigiani, S., Ferrari, P. F., Palanza, P., & Rodgers, R. J. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00373-5 · Cited by 148 · see citing works
Limitations on the use of the C57BL/6 mouse in the tail suspension test
Mayorga, A. J., & Lucki, I. (2001) · Psychopharmacology · doi:10.1007/s002130100687 · Cited by 147 · see citing works
Richter, S. H., Garner, J. P., Zipser, B., Lewejohann, L., Sachser, N., Touma, C., Schindler, B., Chourbaji, S., Brandwein, C., Gass, P., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016461 · Cited by 143 · see citing works
Some critical determinants of the behaviour of rats in the elevated plus-maze
Griebel, G., Moreau, J., Jenck, F., Martin, J. R., & Misslin, R. (1993) · Behavioural Processes · doi:10.1016/0376-6357(93)90026-n · Cited by 139 · see citing works
Natural History of Zebrafish ( Danio rerio ) in India
Arunachalam, M., Raja, M., Vijayakumar, C., Malaiammal, P., & Mayden, R. L. (2013) · Zebrafish · doi:10.1089/zeb.2012.0803 · Cited by 138 · see citing works
Ecological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
Effect of different illumination levels on rat behavior in the elevated plus-maze
Garcia, A. M. B., Cárdenas, F. P., & Morato, S. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.04.007 · Cited by 134 · see citing works
Han, S., Olonisakin, T. F., Pribis, J. P., Zupetic, J., Yoon, J. H., Holleran, K. M., Jeong, K., Shaikh, N., Rubio, D. M., & Lee, J. S. (2017) · PLOS ONE · doi:10.1371/journal.pone.0183591 · Cited by 131 · see citing works
Effects of cage enrichment on behavior, welfare and outcome variability in female mice
Bailoo, J. D., Murphy, E., Boada-Saña, M., Varholick, J. A., Hintze, S., Baussière, C., Hahn, K. C., Göpfert, C., Palme, R., Voelkl, B., et al. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00232 · Cited by 120 · see citing works
Strain- and context-dependent behavioural responses of acute alarm substance exposure in zebrafish
de Quadros, V. A., Silveira, A., Giuliani, G. S., Didonet, F., Silveira, A., Nunes, M. E. M., Silva, T. O., Loro, V. L., & Rosemberg, D. B. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.10.014 · Cited by 117 · see citing works
Paulus, M. P., Dulawa, S. C., Ralph, R. J., & Geyer, M. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01137-3 · Cited by 117 · see citing works
Report Quality of Generalized Linear Mixed Models in Psychology: A Systematic Review
Bono, R., Alarcón, R., & Blanca, M. J. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.666182 · Cited by 115 · see citing works
Handbook of laboratory animal management and welfare
Matfiiiiiiiild, M. (1995) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)89011-2 · Cited by 115 · see citing works
What do zebrafish want? Impact of social grouping, dominance and gender on preference for enrichment
Schroeder, P., Jones, S., Young, I. S., & Sneddon, L. U. (2014) · Laboratory Animals · doi:10.1177/0023677214538239 · Cited by 112 · see citing works
Introducing Therioepistemology: the study of how knowledge is gained from animal research
Garner, J. P., Gaskill, B. N., Weber, E. M., Dallaire, J. A., & Pritchett‐Corning, K. R. (2017) · Lab Animal · doi:10.1038/laban.1224 · Cited by 106 · see citing works
Reproducibility2020: Progress and priorities
Freedman, L. P., Venugopalan, G., & Wisman, R. (2017) · F1000Research · doi:10.12688/f1000research.11334.1 · Cited by 102 · see citing works
Franco, N. H., & Olsson, I. A. S. (2013) · Laboratory Animals · doi:10.1177/0023677213498717 · Cited by 98 · see citing works
Progress toward openness, transparency, and reproducibility in cognitive neuroscience
Gilmore, R. O., Diaz, M. T., Wyble, B. A., & Yarkoni, T. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13325 · Cited by 95 · see citing works
(2012) · InTech eBooks · doi:10.5772/2340 · Cited by 90 · see citing works
Enrichment for Laboratory Zebrafish—A Review of the Evidence and the Challenges
Stevens, C., Reed, B. T., & Hawkins, P. (2021) · Animals · doi:10.3390/ani11030698 · Cited by 84 · see citing works
Strech, D., & Dirnagl, U. (2019) · BMJ Open Science · doi:10.1136/bmjos-2018-000048 · Cited by 79 · see citing works
Pseudoreplication in physiology: More means less
Eisner, D. A. (2021) · The Journal of General Physiology · doi:10.1085/jgp.202012826 · Cited by 79 · see citing works
Festing, M. F. W. (2014) · ILAR Journal · doi:10.1093/ilar/ilu045 · Cited by 78 · see citing works
Aske, K. C., & Waugh, C. A. (2017) · EMBO Reports · doi:10.15252/embr.201744428 · Cited by 75 · see citing works
Systematic heterogenization for better reproducibility in animal experimentation
Richter, S. H. (2017) · Lab Animal · doi:10.1038/laban.1330 · Cited by 69 · see citing works
Effects of light at night on laboratory animals and research outcomes.
Emmer, K. M., Russart, K. L. G., Walker, W. H., Nelson, R. J., & DeVries, A. C. (2018) · Behavioral Neuroscience · doi:10.1037/bne0000252 · Cited by 69 · see citing works
Lee, C. J., Paull, G. C., & Tyler, C. R. (2018) · Journal of Fish Biology · doi:10.1111/jfb.13865 · Cited by 67 · see citing works
Eilam, D., Dank, M., & Maurer, R. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00322-4 · Cited by 61 · see citing works
Voelkl, B., Würbel, H., Krzywinski, M. I., & Altman, N. (2021) · Nature Methods · doi:10.1038/s41592-020-01036-9 · Cited by 57 · see citing works
The Brazilian Reproducibility Initiative
Amaral, O. B., Neves, K., Wasilewska‐Sampaio, A. P., & Carneiro, C. F. D. (2019) · eLife · doi:10.7554/elife.41602 · Cited by 56 · see citing works
The Experimental Design Assistant
du Sert, N. P., Bamsey, I., Bate, S. T., Berdoy, M., Clark, R. A., Cuthill, I. C., Fry, D., Karp, N. A., Macleod, M. R., Moon, L. D. F., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4462 · Cited by 55 · see citing works
The evolution of animal welfare and the 3Rs in Brazil, China, and India.
Bayne, K. A. L., Gudde, R. S., Rivera, E. A. B., & Wang, J. (2015) · PubMed Central · Cited by 51 · see citing works
Experimental Design for Laboratory Biologists
Lazic, S. E. (2016) · Cambridge University Press eBooks · doi:10.1017/9781139696647 · Cited by 50 · see citing works
Synapse formation in adult barrel cortex following naturalistic environmental enrichment
Landers, M. S., Knott, G. W., Lipp, H., Полетаева, И. И., & Welker, E. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.10.040 · Cited by 48 · see citing works
Four simple ways to increase power without increasing the sample size
Lazic, S. (2018) · Laboratory Animals. Journal of the Laboratory Animal Science Association · doi:10.1177/0023677218767478 · Cited by 45 · see citing works
Fong, S., Buechel, S. D., Boussard, A., Kotrschal, A., & Kolm, N. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.200402 · Cited by 44 · see citing works
A Bayesian predictive approach for dealing with pseudoreplication
Lazic, S., Mellor, J., Ashby, M. C., & Munafo, M. (2019) · Scientific Reports · doi:10.1038/s41598-020-59384-7 · Cited by 44 · see citing works
Strech, D., Weissgerber, T. L., Dirnagl, U., & on behalf of QUEST Group (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000576 · Cited by 41 · see citing works
Spatial Cognition and Range Use in Free-Range Laying Hens
Campbell, D. L. M., Talk, A. C., Loh, Z., Dyall, T. R., & Lee, C. (2018) · Animals · doi:10.3390/ani8020026 · Cited by 40 · see citing works
What is the optimum design for my animal experiment?
Karp, N. A., & Fry, D. (2021) · BMJ Open Science · doi:10.1136/bmjos-2020-100126 · Cited by 39 · see citing works
The Contribution of Environmental Enrichment to Phenotypic Variation in Mice and Rats.
Kentner, A. C., Speno, A. V., Doucette, J., & Roderick, R. C. (2021) · eneuro · doi:10.1523/eneuro.0539-20.2021 · Cited by 37 · cited 1× · see citing works
“This last claim has been criticized over the past two decades and suggested to be a fallacy (Wolfer et al., 2004; Kentner et al., 2021; Voelkl et al., 2021).”
BackgroundPseudoreplication is (still) a problem.
Freeberg, T. M., & Lucas, J. R. (2009) · Journal of Comparative Psychology · doi:10.1037/a0017031 · Cited by 37 · see citing works
A three-dimensional habitat for C. elegans environmental enrichment
Guisnet, A., Maitra, M., Pradhan, S., & Hendricks, M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0245139 · Cited by 34 · see citing works
Bertapelle, C., Polese, G., & Cosmo, A. D. (2017) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22735 · Cited by 31 · see citing works
Possamai, F., dos Santos, J., Walber, T., Marcon, J. C., dos Santos, T. S., & de Oliveira, C. L. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.017 · Cited by 31 · see citing works
Lazic, S. E. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1062-7 · Cited by 30 · see citing works
Environmental effects on Drosophila brain development and learning
Wang, X., Amei, A., de Belle, J. S., & Roberts, S. P. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.169375 · Cited by 30 · see citing works
A reaction norm perspective on reproducibility
Voelkl, B., & Würbel, H. (2021) · Theory in Biosciences · doi:10.1007/s12064-021-00340-y · Cited by 29 · see citing works
Melleu, F. F., Pinheiro, M. V., Lino-de-Oliveira, C., & Marino–Neto, J. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1043-6 · Cited by 27 · see citing works
Self-citationTrends and predictors of biomedical research quality, 1990-2015: a meta-research study
Catillon, M. (2019) · BMJ Open · doi:10.1136/bmjopen-2019-030342 · Cited by 27 · see citing works
Behavioral models in psychopathology: epistemic and semantic considerations
Maximino, C., & van der Staay, F. J. (2019) · Behavioral and Brain Functions · doi:10.1186/s12993-019-0152-4 · Cited by 26 · see citing works
Loss, C. M., Binder, L. B., Muccini, E., Martins, W. C., de Oliveira, P. A., Vandresen-Filho, S., Prediger, R. D., Tasca, C. I., Zimmer, E. R., Costa‐Schmidt, L. E., et al. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.016 · Cited by 24 · see citing works
Self-citationTurschwell, M. P., & White, C. R. (2016) · Biology Open · doi:10.1242/bio.015024 · Cited by 22 · see citing works
Environmental enrichment influences neuronal stem cells in the adult crayfish brain
Ayub, N., Benton, J. L., Zhang, Y., & Beltz, B. S. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20864 · Cited by 21 · see citing works
ARRIVEガイドライン2.0:動物研究報告のための更新ガイドライン【JST・京大機械翻訳】
Nathalie, P. D. S., Hurst, V., Ahluwalia, A., Alam, S., Marc, T. A., Baker, M., William, J. B., Alejandra, C., Cuthill, I. C., Ulrich, D., et al. (2020) · British Journal of Pharmacology · Cited by 21 · see citing works
Aging and Aging-Related Diseases: Mechanisms and Interventions
Wang, Z. (2018) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-13-1117-8 · Cited by 21 · see citing works
Steckler, T., Brose, K., Haas, M., Kas, M. J., Koustova, E., & Bespalov, A. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.05.011 · Cited by 20 · see citing works
Refining learning and memory assessment in laboratory rodents. An ethological perspective.
Branchi, I., & Ricceri, L. (2004) · PubMed · Cited by 20 · see citing works
Timing of Environmental Enrichment Affects Memory in the House Cricket, Acheta domesticus
Mallory, H. S., Howard, A. F., & Weiss, M. R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152245 · Cited by 16 · see citing works
Masud, N., Ellison, A., Pope, E. C., & Cable, J. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.229450 · Cited by 16 · see citing works
Addressing selective reporting of experiments through predefined exclusion criteria
Neves, K., & Amaral, O. B. (2020) · eLife · doi:10.7554/elife.56626 · Cited by 15 · see citing works
Neves, K., Carneiro, C. F. D., Wasilewska‐Sampaio, A. P., de Abreu, M. B., Valério‐Gomes, B., Tan, P. B., & Amaral, O. B. (2020) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/0074-02760200328 · Cited by 13 · see citing works
Floating Rodents and Stress-Coping Neurobiology
de Kloet, E. R., & Molendijk, M. L. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.04.003 · Cited by 13 · see citing works
Are happy lab animals better for science?
(2021) · AAAS Articles DO Group · doi:10.1126/science.aat2326 · Cited by 12 · see citing works
Akkerman, S., Prickaerts, J., Bruder, A. K., Wolfs, K. H. M., Vry, J. D., Vanmierlo, T., & Blokland, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0111692 · Cited by 12 · see citing works
Ramos-Hryb, A. B., Cari, H., Aighewi, O., & de Oliveira, C. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.025 · Cited by 12 · see citing works
Are drug targets missed owing to lack of physical activity?
Gurwitz, D. (2001) · Drug Discovery Today · doi:10.1016/s1359-6446(01)01747-0 · Cited by 10 · see citing works
Shkedy, Z., Molenberghs, G., Craenendonck, H. V., Steckler, T., & Bijnens, L. (2005) · Journal of Biopharmaceutical Statistics · doi:10.1081/bip-200049825 · Cited by 9 · see citing works
Time-of-day influence on exploratory behaviour of rats exposed to an unfamiliar environment
Loss, C. M., Córdova, S. D., Callegari-Jacques, S. M., & de Oliveira, D. L. (2014) · Behaviour · doi:10.1163/1568539x-00003224 · Cited by 7 · see citing works
Self-citationBayesian prediction intervals for assessing P-value variability in prospective replication studies
Vsevolozhskaya, O. A., Ruiz, G., & Zaykin, D. V. (2017) · Translational Psychiatry · doi:10.1038/s41398-017-0024-3 · Cited by 5 · see citing works
Shkedy, Z., Vandersmissen, V., Molenberghs, G., Craenendonck, H. V., Aerts, N., Steckler, T., & Bijnens, L. (2005) · Biometrical Journal · doi:10.1002/bimj.200410130 · Cited by 3 · see citing works
The Epistemological (Not Reproducibility) Crisis
Park, J. H. (2020) · Advances in Radiation Oncology · doi:10.1016/j.adro.2020.07.019 · Cited by 3 · see citing works
Ferguson, G. W., Jones, J. R., Gehrmann, W. H., Hammack, S. H., Talent, L. G., Hudson, R. D., Dierenfeld, E. S., Fitzpatrick, M. P., Frye, F. L., Holick, M. F., et al. (1996) · Zoo Biology · doi:10.1002/(sici)1098-2361(1996)15:3
Flagged first, then by citations
1 of the 121 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The grimace scale: a useful tool for assessing pain in laboratory animals
Onuma, K., Watanabe, M., & Sasaki, N. (2024) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.24-0010 · Cited by 23 · see citing works
Blueprints for measuring natural behavior
Puścian, A., & Knapska, E. (2022) · iScience · doi:10.1016/j.isci.2022.104635 · Cited by 21 · see citing works
Klingner, C. M., Denker, M., Grün, S., Hanke, M., Oeltze‐Jafra, S., Ohl, F. W., Radny, J., Rotter, S., Scherberger, H., Stein, A., et al. (2023) · eNeuro · doi:10.1523/eneuro.0215-22.2023 · Cited by 16 · see citing works
Cuff, J. P., Barrett, M., Gray, H., Fox, C. W., Watt, A. D., & Aimé, E. (2024) · Agricultural and Forest Entomology · doi:10.1111/afe.12617 · Cited by 14 · see citing works
Alves, L., Hashiguchi, D., Loss, C. M., van Praag, H., & Longo, B. M. (2025) · Journal of Alzheimer s Disease · doi:10.1177/13872877251321118 · Cited by 12 · see citing works
Self-citationReporting checklists in neuroimaging: promoting transparency, replicability, and reproducibility
Ekhtiari, H., Zare-Bidoky, M., Sangchooli, A., Valyan, A., Abi‐Dargham, A., Cannon, D. M., Carter, C. S., Garavan, H., George, T. P., Ghobadi‐Azbari, P., et al. (2024) · Neuropsychopharmacology · doi:10.1038/s41386-024-01973-5 · Cited by 13 · see citing works
Mösch, L., Kunczik, J., Breuer, L., Merhof, D., Gass, P., Potschka, H., Zechner, D., Vollmar, B., Tolba, R. H., Häger, C., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0286230 · Cited by 9 · see citing works
Neural Circuits of Fear and Anxiety: Insights from a Neuroethological Perspective
Melleu, F. F., & Canteras, N. S. (2024) · Physiology · doi:10.1152/physiol.00042.2024 · Cited by 9 · see citing works
Self-citationIn Vivo Animal Models Development and Their Limitations for Brain Research
Mangrulkar, S. V., Dabhekar, S. V., Neje, P., Parkarwar, N., Turankar, A., Taksande, B. G., Umekar, M. J., & Nakhate, K. T. (2024) · Springer eBooks · doi:10.1007/978-981-97-2859-6_12 · Cited by 9 · see citing works
Pinto, A., Haytural, H., Loss, C. M., Álvarez, C., Ertas, A., Curtis, O., Williams, A. R., Murphy, G., Salleng, K. J., Gografe, S., et al. (2025) · Aging Cell · doi:10.1111/acel.70242 · Cited by 8 · see citing works
Self-citationOne Day Away from Mum has Lifelong Consequences on Brain and Behaviour
de Sá, N. F., Camarini, R., & Suchecki, D. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.06.013 · Cited by 7 · see citing works
Animal welfare assessment after severe traumatic brain injury in rats
Allioux, C., Achaintre, L., Cheataini, F., Balança, B., & Marinesco, S. (2022) · Laboratory Animals · doi:10.1177/00236772221107269 · Cited by 6 · see citing works
Identifying trends in reporting on the ethical treatment of insects in research
Perl, C. D., Kissinger, C., Godfrey, R. K., Castillo, E. M., Fischer, B., & Barrett, M. (2025) · PLoS ONE · doi:10.1371/journal.pone.0328931 · Cited by 5 · see citing works
Bombail, V., Brown, S. M., Beyts, C., Martin, J. E., Li, T., Meddle, S. L., Mendl, M., Robinson, E. S., Hammond, T. J., Nielsen, B. L., et al. (2025) · F1000Research · doi:10.12688/f1000research.166417.2 · Cited by 4 · see citing works
Favoretto, C. A., Bertagna, N. B., Anjos-Santos, A., Loss, C. M., Rodolpho, B. T., Righi, T., Bezerra, F. R., Bianchi, P., & Cruz, F. C. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.11.037 · Cited by 5 · see citing works
Self-citationBertagna, N. B., Favoretto, C. A., Rodolpho, B. T., Righi, T., Loss, C. M., Morais, I. B. M., Vrechi, T. A. D. M., Erustes, A. G., Pereira, G. J. S., Miguel, T. T., et al. (2025) · Alcohol · doi:10.1016/j.alcohol.2025.11.004 · Cited by 3 · see citing works
Self-citationKeller, C., Rading, S., Bîndilă, L., & Karsak, M. (2022) · Cells · doi:10.3390/cells11091517 · Cited by 3 · see citing works
Klingner, C. M., Denker, M., Grün, S., Hanke, M., Oeltze‐Jafra, S., Ohl, F. W., Radny, J., Rotter, S., Scherberger, H., Stein, A., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.07.487439 · Cited by 3 · see citing works
Mösch, L., Kunczik, J., Breuer, L., Merhof, D., Gass, P., Potschka, H., Zechner, D., Vollmar, B., Tolba, R. H., Häager, C., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.12.540546 · Cited by 3 · see citing works
Identifying trends in reporting on the ethical treatment of insects in researchPreprint
Perl, C. D., Kissinger, C., Godfrey, R. K., Castillo, E., Fischer, B., & Barrett, M. (2024) · doi:10.31219/osf.io/hs4gr · Cited by 3 · see citing works
Bombail, V., Brown, S. M., Martin, J., Meddle, S., Mendl, M., Robinson, E. S. J., Hammond, T. J., Nielsen, B. L., LaFollette, M. R., Viñuela-Fernández, I., et al. (2022) · F1000Research · doi:10.12688/f1000research.125649.1 · Cited by 2 · see citing works
Schmidt, R., Welzel, B., & Löscher, W. (2024) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2024.110214 · Cited by 2 · see citing works
Noncontact Video-Based Vital Signs Continuous Monitor for Unconstrained Conscious Rodents
He, Y., Gao, T., Lv, Y., & Zhang, J. (2025) · IEEE Sensors Journal · doi:10.1109/jsen.2025.3557020 · Cited by 2 · see citing works
Editorial: Improving reproducibility in behavioral neuroscience
Loss, C. M., Domingues, K., Sousa, N., & Viola, G. G. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1328525 · Cited by 2 · see citing works
Self-citationMapping the evolution of the forced swim test across interpretation, welfare and pharmacology
Brandwein, C., Leenaars, C. H. C., Iorgu, A.-M., Becker, L., Pfeiffer, N., Vasilescu, A.-N., Cilurzo, C., Bleich, A., Talbot, S. R., Gass, P., et al. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.108146 · Cited by 1 · see citing works
de Sá, N. F., Assad, N., Camarini, R., & Suchecki, D. (2026) · Neurobiology of Stress · doi:10.1016/j.ynstr.2026.100800 · Cited by 1 · see citing works
The emerging field of wild animal welfare science
Elliott, V. L., Beausoleil, N. J., Browning, H., Díez‐León, M., Goddard, P., Graham, M., Ramp, D., Sebo, J., Soryl, A., & Zemanova, M. A. (2026) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2026.06.003 · Cited by 1 · see citing works
Stokes, J. E., Fischer, B., & Barrett, M. (2026) · Ecological Entomology · doi:10.1111/een.70117 · Cited by 1 · see citing works
Stokes, J. E., Fischer, B., & Barrett, M. (2025) · bioRxiv · doi:10.1101/2025.10.21.683772 · Cited by 1 · see citing works
Ferreira, J., Silva, J., Barros, S., Caetano, I., Fernandes, P. A., Olsson, I. A. S., & Valentim, A. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.05.539645
Positive effect of a diggable substrate on the behaviour of a captive naked mole rat colony
Amari, M., Mary, A., Zablocki‐Thomas, P., Bourgeois, A., & Pouydebat, E. (2024) · Scientific Reports · doi:10.1038/s41598-024-64146-w · Cited by 1 · see citing works
Barrios‐Montiel, R., Arteaga, L., Zepeda, J. A., Bautista, A., & Hudson, R. (2025) · Ethology · doi:10.1111/eth.13555
Anésio, A., Costa, G., Palombo, P., Zaniboni, C. R., Yokoyama, T. S., Vialou, V., Loss, C. M., & Cruz, F. C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.17.643658
Self-citationEstimating the Accuracy of Intraperitoneal Drug Administration in Adult Zebrafish
Apukhtin, K. V., Kotova, M. M., Galstyan, D. S., Stewart, A., de Abreu, M. S., & Kalueff, A. V. (2025) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-24-070
Al-Mohammad, H. M. K., Ahmad, H. S., & Alshamarey, D. K. (2025) · Research Square · doi:10.21203/rs.3.rs-6906364/v1
Rearing in a Shelved Environment Chronically Modifies Offspring Behaviour and Physiology
Bigelow, L. J., Pope, E., Ousley, C. G., McGrattan, A. E., MacDonald, D. S., & Bernard, P. B. (2025) · European Journal of Neuroscience · doi:10.1111/ejn.70199
Gili, C., Canestrelli, D., Salvati, E., Fiorito, G., Cerizza, A. F., Cirino, P., Mille, F., Musco, L., Martino, G., Pace, A., et al. (2025) · Reviews in Aquaculture · doi:10.1111/raq.70072
Small Animal Models in Translational Spine Surgery Research
Bonamer, J. P., Bilodeau, R. E., Weinberg, J., Edwards, T., Ramanathan, R., Gonzalez, C., Spitnale, M. J., Lee, J. Y., & Wawrose, R. A. (2025) · Seminars in Spine Surgery · doi:10.1016/j.semss.2025.101235
Caspar-Cohen, J., Demellier, J., Pellé, S., Valenchon, M., Ravel, S., Romain, A., & Petit, O. (2026) · Animal Welfare · doi:10.1017/awf.2026.10061
A Need for Societal Involvement in Promoting a Culture of Care in Animal Research
Azilagbetor, D. M., Shaw, D., Geneviève, L. D., Milford, A., Gaab, J., & Elger, B. S. (2026) · Journal of Bioethical Inquiry · doi:10.1007/s11673-026-10551-x
Strategies for improving the quality and accessibility of captive animal ethograms
Lewis, K., Stupples, K., & Witham, C. (2026) · Frontiers in Ethology · doi:10.3389/fetho.2026.1869694
Düpjan, S., Girard, M., & Westin, R. (2026) · Springer eBooks · doi:10.1007/978-3-032-24899-2_1
Anésio, A., Costa, G. V. L., Palombo, P., Zaniboni, C. R., Yokoyama, T. S., Vialou, V., Loss, C. M., & Cruz, F. C. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.08.047
Self-citationRamos, J., Carrizo, V., Riesco, M. F., Fernández, I., Tort, L., & Khansari, A. R. (2026) · Zebrafish · doi:10.1177/15458547261497048
- Authors
- Loss, C. M., Melleu, F. F., Domingues, K., Lino-de-Oliveira, C., & Viola, G. G.
- Affiliations
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR)
- Universidade de São Paulo (BR)
- Universidade do Porto (PT)
- Corresponding author
- Loss, Cássio Morais
- Venue
- Frontiers in Behavioral Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2021-11-30
- Volume
- 15
- Pages
- 763428-763428
- ISSN
- 1662-5153 (ISSN-L)
- PMC
- PMC8671008
- OpenAlex
- W3215397237
- Cited by
- 44
- References
- 121
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 9 · 2023: 6 · 2022: 5
- FWCI
- 0.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (465458/2014-9 - INCT Translacional em Medicina)
- Fundação de Amparo à Pesquisa do Estado de São Paulo (#2018/25857-5)
- Fundação para a Ciência e a Tecnologia (BIPD/FCT Proj2020/i3S/26040705/2021)
- Alexander von Humboldt-Stiftung (Equipment grants 2019)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal testing and alternatives
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- animal welfare, reproducibility, psychobiology, experimental rigor, animal models, translational medicine
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
