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Research ArticleNew Research, History, Teaching, and Public Awareness

Problems and Progress regarding Sex Bias and Omission in Neuroscience Research

Tyler R. Will, Stephanie B. Proaño, Anly M. Thomas, Lindsey M. Kunz, Kelly C. Thompson, Laura A. Ginnari, Clay H. Jones, Sarah-Catherine Lucas, Elizabeth M. Reavis, David M. Dorris and John Meitzen
eNeuro 3 November 2017, 4 (6) ENEURO.0278-17.2017; https://doi.org/10.1523/ENEURO.0278-17.2017
Tyler R. Will
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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Stephanie B. Proaño
2Graduate Program in Zoology, North Carolina State University, Raleigh, NC
3W.M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC
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Anly M. Thomas
4Graduate Program in Physiology, North Carolina State University, Raleigh, NC
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Lindsey M. Kunz
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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Kelly C. Thompson
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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Laura A. Ginnari
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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Clay H. Jones
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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Sarah-Catherine Lucas
5Department of Psychology, North Carolina State University, Raleigh, NC
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Elizabeth M. Reavis
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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David M. Dorris
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
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John Meitzen
1Department of Biological Sciences, North Carolina State University, Raleigh, NC
3W.M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC
6Center for Human Health and the Environment, North Carolina State University, Raleigh, NC
7Comparative Medicine Institute, North Carolina State University, Raleigh, NC
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    Figure 1.

    Articles using mice and rats are a significant and stable proportion of the neuroscience literature. A, From 2010 to 2014, 13,857 neuroscience research articles were published by the J. Neurosci., J. Neurophysiol., Nat. Neurosci., Neuron, Science, and Nature (gray bar). Of these articles, 6,636 used rats or mice and were further analyzed (purple bar). The total number of articles using mice and rats was consistently distributed across years. B, The percentage of articles using rats or mice remained fairly constant across years.

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    Figure 2.

    Sex omission is decreasing but sex bias remains present, with different patterns observed in articles using mice versus those using rats. Articles were categorized as either not reporting sex (orange) or reporting both males and females (red), only males (green), or only females (blue). A, All articles, using both mice and rats. Articles not reporting animal sex decreased from 2010 to 2014. Articles using only male animals increased from 2010 to 2014, comprising the largest proportion of articles by 2011. Articles reporting the use of both male and female animals also increased over time, nearing but not overtaking the percentage of articles using only males by 2013. Articles using only female animals remained stable and low. B, Mice. Articles not reporting mice sex decreased from 2010 to 2014. Articles reporting the use of both male and female mice increased over time and comprised the largest proportion of articles by 2012. Articles using only male mice increased from 2010 to 2014. Articles using only female mice remained stable and low. C, Rats. Articles not reporting rat sex decreased from 2010 to 2014. Article using only male rats increased from 2010 to 2014 and comprised the largest proportion of articles by 2011. Articles reporting the use of both male and female rats increased from 2010 to 2014, but were a much smaller proportion of the dataset than articles using only male rats. Articles using only female rats remained stable and low.

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    Figure 3.

    The vast majority of articles using both male and female animals do not report analyzing sex as an experimental variable. Articles using both male and female animals were evaluated for any formal statistical test or statement that data from males and females were compared, regardless of outcome and whether or not data were reported. The overall percentage of articles incorporating sex as an experimental variable remained low and relatively stable from 2011 to 2014 (∼14%), after a noticeable decrease from the year 2010 (25%).

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    Figure 4.

    Sex omission and bias differ by journal and change from 2010 to 2014. Articles were analyzed from the following journals: J. Neurosci., J. Neurophysiol., Nat. Neurosci., Neuron, Science, and Nature. Four of the six journals showed large decreases in sex omission. Of this group, Neuron showed the smallest decrease, beginning with 69% of articles not reporting sex in 2010, decreasing to 55% in 2014. In contrast, one journal, Science, showed an increase in the percentage of articles not reporting sex, rising from 51% in 2010% to 58% in 2014.

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    Figure 5.

    Patterns of sex omission and bias markedly differ across years by journal. A, Articles not reporting sex. The percentage of articles not reporting sex decreased in five of six journals. The percentage of articles not reporting sex increased in the journal Science. The journals Science and Neuron showed high percentages of articles not reporting sex. B, Articles reporting both males and females. Most journals show increased percentages of articles reporting both males and females, although different patterns occur across time. C, Articles reporting only males. D, Articles reporting only females. The percentage of articles reporting the sole use of female animals remained stable and low in all journals. Green, J. Neurosci.; black, J. Neurophysiol.; blue, Nat. Neurosci.; red, Neuron; orange, Science; purple, Nature.

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    Table 1.

    Details of statistical analysis

    FigureData structureType of testConfidence intervals
    1BNormal distributionLinear regression–4.389 to 3.178
    2ANormal distributionLinear regressionMale only: 0.8086 to 3.575; female only: –0.5272 to 1.069; male and female: 1.277 to 8.273; unspecified sex: –12.64 to –1.834
    2BNormal distributionLinear regressionMale only: 1.105 to 2.797; female only: –0.5271 to 1.073; male and female: 2.294 to 8.554; unspecified sex: –12.16 to –3.138
    2CNormal distributionLinear regressionMale only: 1.197 to 6.233; female only: –0.1067 to 0.8067; male and female: –1.040 to 7.242; unspecified sex: –13.97 to –0.3654
    3Normal distributionLinear regression–6.877 to 2.767
    5ANormal distributionLinear regression, ANCOVAJ. Neurophysiol.: –10.05 to –1.779; J. Neurosci.: –16.76 to 0.5671; Nature: –18.14 to –8.113; Nat. Neurosci.: –21.17 to –1.192; Neuron: –4.831 to –1.845; Science: –8.771 to 12.49
    5BNormal distributionLinear regression, ANCOVAJ. Neurophysiol.: 0.03390 to 5.726; J. Neurosci.: –0.8596 to 11.99; Nature: 1.781 to 22.73; Nat. Neurosci.: –1.290 to 9.552; Neuron: –0.5016 to 5.360; Science: –8.859 to 9.249
    5CNormal distributionLinear regression, ANCOVAJ. Neurophysiol.: –0.4495 to 6.815; J. Neurosci.: 0.3678 to 3.688; Nature: –5.311 to 7.824; Nat. Neurosci.: –0.6518 to 13.34; Neuron: –1.601 to 3.571; Science: –11.46 to 8.715
    5DNormal distributionLinear regression, ANCOVAJ. Neurophysiol.: –0.5273 to 0.2373; J. Neurosci.: –2.637 to 1.863; Nature: –2.637 to 1.862; Nat. Neurosci.: –1.188 to 2.426; Neuron: –2.402 to 2.252; Science: –4.550 to 3.180
    • Confidence intervals for linear regressions indicate the 95% confidence interval surrounding the slope. R 2 and other relevant statistics are reported in Results. ANCOVA, analysis of covariance.

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Problems and Progress regarding Sex Bias and Omission in Neuroscience Research
Tyler R. Will, Stephanie B. Proaño, Anly M. Thomas, Lindsey M. Kunz, Kelly C. Thompson, Laura A. Ginnari, Clay H. Jones, Sarah-Catherine Lucas, Elizabeth M. Reavis, David M. Dorris, John Meitzen
eNeuro 3 November 2017, 4 (6) ENEURO.0278-17.2017; DOI: 10.1523/ENEURO.0278-17.2017

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Problems and Progress regarding Sex Bias and Omission in Neuroscience Research
Tyler R. Will, Stephanie B. Proaño, Anly M. Thomas, Lindsey M. Kunz, Kelly C. Thompson, Laura A. Ginnari, Clay H. Jones, Sarah-Catherine Lucas, Elizabeth M. Reavis, David M. Dorris, John Meitzen
eNeuro 3 November 2017, 4 (6) ENEURO.0278-17.2017; DOI: 10.1523/ENEURO.0278-17.2017
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