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Research Article

Sex beyond the genitalia: The human brain mosaic

Daphna Joel, Zohar Berman, Ido Tavor, Nadav Wexler, Olga Gaber, Yaniv Stein, Nisan Shefi, Jared Pool, Sebastian Urchs, Daniel S. Margulies, Franziskus Liem, Jürgen Hänggi, Lutz Jäncke, and Yaniv Assaf
  1. aSchool of Psychological Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
  2. bSagol School of Neuoroscience, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
  3. cDepartment of Neurobiology, Faculty of Life Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
  4. dSchool of Mathematical Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
  5. eMax Planck Research Group for Neuroanatomy & Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany;
  6. fDivision Neuropsychology, Department of Psychology, University of Zurich, 8050 Zurich, Switzerland

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PNAS December 15, 2015 112 (50) 15468-15473; first published November 30, 2015; https://doi.org/10.1073/pnas.1509654112
Daphna Joel
aSchool of Psychological Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
bSagol School of Neuoroscience, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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  • For correspondence: djoel@post.tau.ac.il
Zohar Berman
bSagol School of Neuoroscience, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Ido Tavor
cDepartment of Neurobiology, Faculty of Life Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Nadav Wexler
dSchool of Mathematical Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Olga Gaber
aSchool of Psychological Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Yaniv Stein
dSchool of Mathematical Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Nisan Shefi
aSchool of Psychological Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
bSagol School of Neuoroscience, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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Jared Pool
eMax Planck Research Group for Neuroanatomy & Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany;
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Sebastian Urchs
eMax Planck Research Group for Neuroanatomy & Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany;
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Daniel S. Margulies
eMax Planck Research Group for Neuroanatomy & Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany;
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Franziskus Liem
eMax Planck Research Group for Neuroanatomy & Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany;
fDivision Neuropsychology, Department of Psychology, University of Zurich, 8050 Zurich, Switzerland
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Jürgen Hänggi
fDivision Neuropsychology, Department of Psychology, University of Zurich, 8050 Zurich, Switzerland
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Lutz Jäncke
fDivision Neuropsychology, Department of Psychology, University of Zurich, 8050 Zurich, Switzerland
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Yaniv Assaf
bSagol School of Neuoroscience, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
cDepartment of Neurobiology, Faculty of Life Sciences, Tel-Aviv University, Ramat Aviv, Tel-Aviv 6997801, Israel;
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  1. Edited by Bruce S. McEwen, The Rockefeller University, New York, NY, and approved October 23, 2015 (received for review June 4, 2015)

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Significance

Sex/gender differences in the brain are of high social interest because their presence is typically assumed to prove that humans belong to two distinct categories not only in terms of their genitalia, and thus justify differential treatment of males and females. Here we show that, although there are sex/gender differences in brain and behavior, humans and human brains are comprised of unique “mosaics” of features, some more common in females compared with males, some more common in males compared with females, and some common in both females and males. Our results demonstrate that regardless of the cause of observed sex/gender differences in brain and behavior (nature or nurture), human brains cannot be categorized into two distinct classes: male brain/female brain.

Abstract

Whereas a categorical difference in the genitals has always been acknowledged, the question of how far these categories extend into human biology is still not resolved. Documented sex/gender differences in the brain are often taken as support of a sexually dimorphic view of human brains (“female brain” or “male brain”). However, such a distinction would be possible only if sex/gender differences in brain features were highly dimorphic (i.e., little overlap between the forms of these features in males and females) and internally consistent (i.e., a brain has only “male” or only “female” features). Here, analysis of MRIs of more than 1,400 human brains from four datasets reveals extensive overlap between the distributions of females and males for all gray matter, white matter, and connections assessed. Moreover, analyses of internal consistency reveal that brains with features that are consistently at one end of the “maleness-femaleness” continuum are rare. Rather, most brains are comprised of unique “mosaics” of features, some more common in females compared with males, some more common in males compared with females, and some common in both females and males. Our findings are robust across sample, age, type of MRI, and method of analysis. These findings are corroborated by a similar analysis of personality traits, attitudes, interests, and behaviors of more than 5,500 individuals, which reveals that internal consistency is extremely rare. Our study demonstrates that, although there are sex/gender differences in the brain, human brains do not belong to one of two distinct categories: male brain/female brain.

  • gender differences
  • sex differences
  • brain structure
  • brain connectivity
  • behavior

Footnotes

  • ↵1To whom correspondence should be addressed. Email: djoel{at}post.tau.ac.il.
  • Author contributions: D.J. designed research; D.J., Z.B., S.U., F.L., J.H., and L.J. performed research; D.J. and Y.A. contributed new analytic tools; D.J., Z.B., I.T., N.W., O.G., Y.S., N.S., J.P., S.U., F.L., and J.H. analyzed data; and D.J. and D.S.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Our anonymized raw neuroimaging data and accompanying metadata have been deposited at psy-neuro-nassy.uzh.ch and are accessible with a username and password that can be obtained from the authors by email (djoel{at}post.tau.ac.il or j.haenggi{at}psychologie.uzh.ch).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1509654112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Sex beyond the genitalia: The human brain mosaic
Daphna Joel, Zohar Berman, Ido Tavor, Nadav Wexler, Olga Gaber, Yaniv Stein, Nisan Shefi, Jared Pool, Sebastian Urchs, Daniel S. Margulies, Franziskus Liem, Jürgen Hänggi, Lutz Jäncke, Yaniv Assaf
Proceedings of the National Academy of Sciences Dec 2015, 112 (50) 15468-15473; DOI: 10.1073/pnas.1509654112

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Sex beyond the genitalia: The human brain mosaic
Daphna Joel, Zohar Berman, Ido Tavor, Nadav Wexler, Olga Gaber, Yaniv Stein, Nisan Shefi, Jared Pool, Sebastian Urchs, Daniel S. Margulies, Franziskus Liem, Jürgen Hänggi, Lutz Jäncke, Yaniv Assaf
Proceedings of the National Academy of Sciences Dec 2015, 112 (50) 15468-15473; DOI: 10.1073/pnas.1509654112
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This article has Letters. Please see:

  • Relationship between Research Article and Letter - March 16, 2016
  • Relationship between Research Article and Letter - March 08, 2016
  • Relationship between Research Article and Letter - March 16, 2016
  • Relationship between Research Article and Letter - March 16, 2016

See related content:

  • Sex differences in the brain do not “add up”
    - Mar 08, 2016
  • Do brains belong to two distinct populations?
    - Mar 16, 2016
Proceedings of the National Academy of Sciences: 112 (50)
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