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Triangulating the sexually dimorphic brain through high-resolution neuroimaging of murine sex chromosome aneuploidies

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Abstract

Murine sex chromosome aneuploidies (SCAs) provide powerful models for charting sex chromosome influences on mammalian brain development. Here, building on prior work in X-monosomic (XO) mice, we use spatially non-biased high-resolution imaging to compare and contrast neuroanatomical alterations in XXY and XO mice relative to their wild-type XX and XY littermates. First, we show that carriage of a supernumerary X chromosome in XXY males (1) does not prevent normative volumetric masculinization of the bed nucleus of the stria terminalis (BNST) and medial amygdala, but (2) causes distributed anatomical alterations relative to XY males, which show a statistically unexpected tendency to be co-localized with and reciprocal to XO-XX differences in anatomy. These overlaps identify the lateral septum, BNST, ventral group thalamic nuclei and periaqueductal gray matter as regions with replicable sensitivity to X chromosome dose across two SCAs. We then harness anatomical variation across all four karyotype groups in our study—XO, XX, XY and XXY—to create an agnostic data-driven segmentation of the mouse brain into five distributed clusters which (1) recover fundamental properties of brain organization with high spatial precision, (2) define two previously uncharacterized systems of relative volume excess in females vs. males (“forebrain cholinergic” and “cerebelo-pontine-thalamo-cortical”), and (3) adopt stereotyped spatial motifs which delineate ordered gradients of sex chromosome and gonadal influences on volumetric brain development. Taken together, these data provide a new framework for the study of sexually dimorphic influences on brain development in health and disrupted brain development in SCA.

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Authors and Affiliations

  1. Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Rm 4C108, Building 20, 10 Center Drive, Bethesda, MD, 20815, USA

    Armin Raznahan, Deanna Greenstein & Jay Giedd

  2. Division of Endocrinology, Department of Medicine, Los Angele Biomedical Research Institute at Harbor-UCLA Medical Center, Torrance, CA, USA

    YanHe Lue, Christina Wang & Ronald Swerdloff

  3. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA

    Frank Probst

  4. Mouse Imaging Centre and Program in Neuroscience and Mental, The Hospital for Sick Children Hospital, Toronto, ON, Canada

    Jason Lerch

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  1. Armin Raznahan
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  2. YanHe Lue
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Correspondence to Armin Raznahan.

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J. Lerch and R. Swerdloff contributed equally to this work.

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Raznahan, A., Lue, Y., Probst, F. et al. Triangulating the sexually dimorphic brain through high-resolution neuroimaging of murine sex chromosome aneuploidies. Brain Struct Funct 220, 3581–3593 (2015). https://doi.org/10.1007/s00429-014-0875-9

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