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Doublecortin-Expressing Neurons in Human Cerebral Cortex Layer II and Amygdala from Infancy to 100 Years Old

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Abstract

A cohort of morphologically heterogenous doublecortin immunoreactive (DCX +) “immature neurons” has been identified in the cerebral cortex largely around layer II and the amygdala largely in the paralaminar nucleus (PLN) among various mammals. To gain a wide spatiotemporal view on these neurons in humans, we examined layer II and amygdalar DCX + neurons in the brains of infants to 100-year-old individuals. Layer II DCX + neurons occurred throughout the cerebrum in the infants/toddlers, mainly in the temporal lobe in the adolescents and adults, and only in the temporal cortex surrounding the amygdala in the elderly. Amygdalar DCX + neurons occurred in all age groups, localized primarily to the PLN, and reduced in number with age. The small-sized DCX + neurons were unipolar or bipolar, and formed migratory chains extending tangentially, obliquely, and inwardly in layers I–III in the cortex, and from the PLN to other nuclei in the amygdala. Morphologically mature-looking neurons had a relatively larger soma and weaker DCX reactivity. In contrast to the above, DCX + neurons in the hippocampal dentate gyrus were only detected in the infant cases in parallelly processed cerebral sections. The present study reveals a broader regional distribution of the cortical layer II DCX + neurons than previously documented in human cerebrum, especially during childhood and adolescence, while both layer II and amygdalar DCX + neurons persist in the temporal lobe lifelong. Layer II and amygdalar DCX + neurons may serve as an essential immature neuronal system to support functional network plasticity in human cerebrum in an age/region-dependent manner.

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Data Availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the supplemental data. Upon reasonable request, additional experimental data and materials for this study can be requested at the discretion of the corresponding author.

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Acknowledgements

We would like to express our greatest gratitude and respect to the individuals who donate their brains to help understand human brain health and diseases.

Funding

This study was supported by National Natural Science Foundation of China (#82071223), Ministry of Science and Technology of China (STI2030-Major Projects#2021ZD0201103 and #2021ZD0201803), and Hunan Provincial Science and Technology Foundation (#2018JJ2552 and #2022JJ40817).

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  1. Ya-Nan Li and Dan-Dan Hu contribute equally to this work.

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Central South University Xiangya Medical School, Changsha, 410013, Hunan, China

    Ya-Nan Li, Dan-Dan Hu, Xiao-Lu Cai, Yan Wang, Chen Yang, Juan Jiang, Qi-Lei Zhang, Tian Tu, Xiao-Sheng Wang, Hui Wang, Aihua Pan, Xiao-Xin Yan & Lily Wan

  2. Department of Neurology, Xiangya Hospital, Central South University, Changsha, 410008, Hunan, China

    Tian Tu

  3. Department of Neurology, Brain Hospital of Hunan Province, Changsha, 410007, Hunan, China

    Ewen Tu

  4. Department of Psychiatry, The Second Xiangya Hospital, Central South University, Changsha, 410031, Hunan, China

    Xiao-Ping Wang

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Contributions

Conceptualization, Lily Wan, Aihua Pan, and Xiao-Xin Yan. Data curation, Ya-Nan Li and Dan-Dan Hu. Funding acquisition, Lily-Wan, Ewen Tu, Xiao-Sheng Wang, Hui Wang, Xiao-Ping Wang, and Xiao-Xin Yan. Methodology, Ya-Nan Li, Dan-Dan Hu, Xiao-Lu Cai, Yan Wang, Chen Yang, Juan Jiang, Qi-Lei Zhang, Tian Tu. Writing—original draft, Lily Wan. Writing—review and editing, Aihua Pan and Xiao-Xin Yan.

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Correspondence to Aihua Pan or Lily Wan.

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The use of postmodern human brains was approved by the Ethics Committee for Research and Education at Xiangya School of Medicine, in compliance with the Code of Ethics of the World Medical Association (Declaration of Helsinki). Written informed consent for body/brain donation was obtained by the willed body donation center of Xiangya School of Medicine.

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Li, YN., Hu, DD., Cai, XL. et al. Doublecortin-Expressing Neurons in Human Cerebral Cortex Layer II and Amygdala from Infancy to 100 Years Old. Mol Neurobiol 60, 3464–3485 (2023). https://doi.org/10.1007/s12035-023-03261-7

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