Protracted neuronal recruitment in the temporal lobes of young children

Marcos Assis Nascimento, Sean Biagiotti, Vicente Herranz-Pérez, Samara Santiago, Raymund Bueno, Chun J. Ye, Taylor J. Abel, Zhuangzhi Zhang, Juan S. Rubio-Moll, Arnold R. Kriegstein, Zhengang Yang, Jose Manuel Garcia-Verdugo, Eric J. Huang, Arturo Alvarez-Buylla, Shawn F. Sorrells

Abstract

The temporal lobe of the human brain contains the entorhinal cortex (EC). This region of the brain is a highly interconnected integrative hub for sensory and spatial information; it also has a key role in episodic memory formation and is the main source of cortical hippocampal inputs1,2,3,4. The human EC continues to develop during childhood5, but neurogenesis and neuronal migration to the EC are widely considered to be complete by birth. Here we show that the human temporal lobe contains many young neurons migrating into the postnatal EC and adjacent regions, with a large tangential stream persisting until the age of around one year and radial dispersal continuing until around two to three years of age. By contrast, we found no equivalent postnatal migration in rhesus macaques (Macaca mulatta). Immunostaining and single-nucleus RNA sequencing of ganglionic eminence germinal zones, the EC stream and the postnatal EC revealed that most migrating cells in the EC stream are derived from the caudal ganglionic eminence and become LAMP5+RELN+ inhibitory interneurons. These late-arriving interneurons could continue to shape the processing of sensory and spatial information well into postnatal life, when children are actively interacting with their environment. The EC is one of the first regions of the brain to be affected in Alzheimer’s disease, and previous work has linked cognitive decline to the loss of LAMP5+RELN+ cells6,7. Our investigation reveals that many of these cells arrive in the EC through a major postnatal migratory stream in early childhood.

Datasets

1. Subpallial germinal zones and the developing human entorhinal cortex
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H4612544 cells
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dEC11050 cells
H2911034 cells
CGE8561 cells
hsb2378445 cells
H488363 cells
H717814 cells
EC Stream7618 cells
H316948 cells
LGE6064 cells
MGE6052 cells
H375869 cells
hsb6284559 cells
H394033 cells
H333420 cells
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Protracted neuronal recruitment in the temporal lobes of young children
2. Interneuron maturation in the human entorhinal cortex
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dEC3054 cells
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hsb2371402 cells
LGE1285 cells
H481117 cells
H311046 cells
EC Stream849 cells
hsb628788 cells
H33570 cells
H39565 cells
MGE418 cells
H37236 cells
Preview
Protracted neuronal recruitment in the temporal lobes of young children
3. EC Stream Region at 14 days of age
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manaab_H717618 cells
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Protracted neuronal recruitment in the temporal lobes of young children

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Source data

https://cellxgene.cziscience.com/collections/cae8bad0-39e9-4771-85a7-822b0e06de9f

Alias names

PMID38122823, PMC10901738

Cite this study

Nascimento, M.A., Biagiotti, S., Herranz-Pérez, V., Santiago, S., Bueno, R., Ye, C.J., Abel, T.J., Zhang, Z., Rubio-Moll, J.S., Kriegstein, A.R. and Yang, Z., 2024. Protracted neuronal recruitment in the temporal lobes of young children. Nature, 626(8001), pp.1056-1065. https://doi.org/10.1038/s41586-023-06981-x