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Articles, Systems/Circuits

Female-Specific Intergenerational Transmission Patterns of the Human Corticolimbic Circuitry

Bun Yamagata, Kou Murayama, Jessica M. Black, Roeland Hancock, Masaru Mimura, Tony T. Yang, Allan L. Reiss and Fumiko Hoeft
Journal of Neuroscience 27 January 2016, 36 (4) 1254-1260; https://doi.org/10.1523/JNEUROSCI.4974-14.2016
Bun Yamagata
1Center for Interdisciplinary Brain Sciences Research, Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California 94305,
2Department of Neuropsychiatry, Keio University School of Medicine, Tokyo 160-8582, Japan,
3Department of Neuropsychiatry, Showa University School of Medicine, Tokyo 157-8577, Japan,
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Kou Murayama
4Department of Psychology, University of Reading, Whiteknights, Reading RG6 6AL, United Kingdom,
5Research Unit of Psychology, Education, and Technology, Kochi University of Technology, Kochi 782-8502, Japan,
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Jessica M. Black
6Graduate School of Social Work, Boston College, Chestnut Hill, Massachusetts 02467, and
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Roeland Hancock
7Division of Child and Adolescent Psychiatry, Department of Psychiatry, University of California San Francisco, San Francisco, California 94143
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Masaru Mimura
2Department of Neuropsychiatry, Keio University School of Medicine, Tokyo 160-8582, Japan,
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Tony T. Yang
7Division of Child and Adolescent Psychiatry, Department of Psychiatry, University of California San Francisco, San Francisco, California 94143
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Allan L. Reiss
1Center for Interdisciplinary Brain Sciences Research, Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California 94305,
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Fumiko Hoeft
2Department of Neuropsychiatry, Keio University School of Medicine, Tokyo 160-8582, Japan,
7Division of Child and Adolescent Psychiatry, Department of Psychiatry, University of California San Francisco, San Francisco, California 94143
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Abstract

Parents have large genetic and environmental influences on offspring's cognition, behavior, and brain. These intergenerational effects are observed in mood disorders, with particularly robust association in depression between mothers and daughters. No studies have thus far examined the neural bases of these intergenerational effects in humans. Corticolimbic circuitry is known to be highly relevant in a wide range of processes, including mood regulation and depression. These findings suggest that corticolimbic circuitry may also show matrilineal transmission patterns. Therefore, we examined human parent–offspring association in this neurocircuitry and investigated the degree of association in gray matter volume between parent and offspring. We used voxelwise correlation analysis in a total of 35 healthy families, consisting of parents and their biological offspring. We found positive associations of regional gray matter volume in the corticolimbic circuit, including the amygdala, hippocampus, anterior cingulate cortex, and ventromedial prefrontal cortex between biological mothers and daughters. This association was significantly greater than mother–son, father–daughter, and father–son associations. The current study suggests that the corticolimbic circuitry, which has been implicated in mood regulation, shows a matrilineal-specific transmission patterns. Our preliminary findings are consistent with what has been found behaviorally in depression and may have clinical implications for disorders known to have dysfunction in mood regulation such as depression. Studies such as ours will likely bridge animal work examining gene expression in the brains and clinical symptom-based observations and provide promising ways to investigate intergenerational transmission patterns in the human brain.

SIGNIFICANCE STATEMENT Parents have large genetic and environmental influences on the offspring, known as intergenerational effects. Specifically, depression has been shown to exhibit strong matrilineal transmission patterns. Although intergenerational transmission patterns in the human brain are virtually unknown, this would suggest that the corticolimbic circuitry relevant to a wide range of processes including mood regulation may also show matrilineal transmission patterns. Therefore, we examined the degree of association in corticolimbic gray matter volume (GMV) between parent and offspring in 35 healthy families. We found that positive correlations in maternal corticolimbic GMV with daughters were significantly greater than other parent–offspring dyads. Our findings provide new insight into the potential neuroanatomical basis of circuit-based female-specific intergenerational transmission patterns in depression.

  • anxiety disorder
  • MRI
  • intergenerational imaging
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The Journal of Neuroscience: 36 (4)
Journal of Neuroscience
Vol. 36, Issue 4
27 Jan 2016
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Female-Specific Intergenerational Transmission Patterns of the Human Corticolimbic Circuitry
Bun Yamagata, Kou Murayama, Jessica M. Black, Roeland Hancock, Masaru Mimura, Tony T. Yang, Allan L. Reiss, Fumiko Hoeft
Journal of Neuroscience 27 January 2016, 36 (4) 1254-1260; DOI: 10.1523/JNEUROSCI.4974-14.2016

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Female-Specific Intergenerational Transmission Patterns of the Human Corticolimbic Circuitry
Bun Yamagata, Kou Murayama, Jessica M. Black, Roeland Hancock, Masaru Mimura, Tony T. Yang, Allan L. Reiss, Fumiko Hoeft
Journal of Neuroscience 27 January 2016, 36 (4) 1254-1260; DOI: 10.1523/JNEUROSCI.4974-14.2016
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Keywords

  • anxiety disorder
  • MRI
  • intergenerational imaging

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