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Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data

Jonasson, Zachariah·2005·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2004.10.006

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Abstract

The existence of sex differences in the standard rat and mouse models of learning and memory is a controversial and contested topic in the literature. The present meta-analysis of radial maze and water maze experiments was conducted to assess the reliablility and magnitude of sex effects in the standard rodent models of learning and memory. Data were culled from published and unpublished sources. Findings indicate large reliable male advantages for rats in radial maze and water maze protocols. Significant strain differences were also identified. In each paradigm, protocol variations were associated with differential sex effects. For the water maze, smaller male advantages were associated with pretraining regimens and for the radial maze, larger significant male advantages were observed in protocols that included unbaited arms (combined reference and working memory protocols). Mouse studies exhibited a different pattern of sex effects; small female advantages were evident in the water maze, but small male advantages were evident in the radial maze. Together these findings establish the reliability of male advantages in spatial working and reference memory for rats across strains, protocols, ages and rearing environments. The findings also support an important species dichotomy between rats and mice that should be considered when transitioning from rat to mouse models. In light of these results, the biological evidence supporting theoretical explanations of sex differences is reviewed and evaluated.

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Cohen, J. (1990) · Computers Environment and Urban Systems · doi:10.1016/0198-9715(90)90050-4 · Cited by 65,417
Statistical Power Analysis for the Behavioral Sciences (2nd ed.).
Lachenbruch, P. A., & Cohen, J. (1989) · Journal of the American Statistical Association · doi:10.2307/2290095 · Cited by 37,421
Book Reviews: Statistical Methods for Meta-Analysis Larry V. Hedges and Ingram Olkin New York: Academic Press, 1985. xxii + 369 pp
Wasserman, S. S., Hedges, L. V., & Olkin, I. (1988) · Journal of Educational Statistics · doi:10.2307/1164953 · Cited by 10,377
The file drawer problem and tolerance for null results.
Rosenthal, R. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.3.638 · Cited by 9,068
Meta-Analytic Procedures for Social Research
Rosenthal, R. (1991) · doi:10.4135/9781412984997 · Cited by 4,635
Meta-Analytic Procedures for Social Research.
Metcalfe, A., & Rosenthal, R. (1994) · Journal of the Royal Statistical Society Series D (The Statistician) · doi:10.2307/2348600 · Cited by 4,249
Essentials of Behavioral Research: Methods and Data Analysis
Rosenthal, R., & Rosnow, R. L. (1984) · Cited by 3,925
Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables
Voyer, D., Voyer, S., & Bryden, M. P. (1995) · Psychological Bulletin · doi:10.1037/0033-2909.117.2.250 · Cited by 2,868
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Morris, R. G. M. (1981) · Learning and Motivation · doi:10.1016/0023-9690(81)90020-5 · Cited by 2,699
Statistical Methods for Meta-Analysis
(1985) · Elsevier eBooks · doi:10.1016/c2009-0-03396-0 · Cited by 2,570

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Authors: Jonasson, Z.
Affiliations: Harvard University (US)
Corresponding author: Jonasson, Zachariah
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2005-01
Volume: 28
Issue: 8
Pages: 811-825
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2004.10.006
OpenAlex: W2086252264
Cited by: 498
References: 106
Citations by year: 2026: 8 · 2025: 17 · 2024: 11 · 2023: 20 · 2022: 29 · 2021: 34 · 2020: 26 · 2019: 29 · 2018: 26 · 2017: 22 · 2016: 25 · 2015: 27 · 2014: 21 · 2013: 39 · 2012: 26
FWCI: 1.62
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: Harvard University
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: sex differences, learning and memory, spatial memory, radial maze, water maze, rats, mice, strain differences, working memory, reference memory, pre-training, species differences, rearing conditions, age effects
MeSH terms: Animals, Behavior, Animal, Learning, Memory, Rodentia, Sex Characteristics, Maze Learning, Models, Animal

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Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data

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