Regulation of Prefrontal Patterning, Connectivity and Synaptogenesis by Retinoic Acid
Open accessAbstract
The prefrontal cortex (PFC) and its reciprocal connections with the mediodorsal thalamus (MD) are crucial for cognitive flexibility and working memory 1–4 and are thought to be altered in several disorders such as autism spectrum disorder 5, 6 and schizophrenia 6–9 . While developmental mechanisms governing regional patterning of the rodent cerebral cortex have been characterized 10–15 , the mechanisms underlying the development of PFC-MD connectivity and the lateral expansion of PFC with distinct granular layer 4 in anthropoid primates 16–23 have not been elucidated. Here we report increased concentration of retinoic acid (RA), a signaling molecule involved in brain development and function 24, 25 in the prospective PFC areas of human and macaque, compared to mouse, during mid-fetal development, a crucial period for cortical circuit assembly. In addition, we observed the lateral expansion of RA synthesizing enzyme, ALDH1A3, expression in mid-fetal macaque and human frontal cortex, compared to mouse. Furthermore, we found that enrichment of RA signaling is restricted to the prospective PFC by CYP26B1 , a gene encoding an RA-catabolizing enzyme upregulated in the mid-fetal motor cortex. Gene deletion in mice revealed that RA signaling through anteriorly upregulated RA receptors, Rxrg and Rarb , and Cyp26b1 -dependent catabolism is required for the proper molecular patterning of PFC and motor areas, the expression of the layer 4 marker RORB , intra-PFC synaptogenesis, and the development of reciprocal PFC-MD connectivity. Together, these findings reveal a critical role for RA signaling in PFC development and, potentially, its evolutionary expansion.
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Retinoic acid (RA) plays a critical role in PFC development and specifically in thalamus-prefrontal connectivity.
“Recently it was found that retinoic acid (RA) plays a critical role in PFC development and specifically in this thalamus-prefrontal connectivity [203].”
From Development of prefrontal cortex (2022) · cites this paper as [203]
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Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“Recently it was found that retinoic acid (RA) plays a critical role in PFC development and specifically in this thalamus-prefrontal connectivity [203].”
BackgroundThree-dimensional genome rewiring in loci with human accelerated regions
Keough, K. C., Whalen, S., Inoue, F., Przytycki, P. F., Fair, T., Deng, C., Steyert, M., Ryu, H., Lindblad-Toh, K., Karlsson, E., et al. (2023) · Science · doi:10.1126/science.abm1696 · Cited by 113 · see citing works
- Authors
- Shibata, M., Pattabiraman, K., Lorente-Galdos, B., Andrijevic, D., Xing, X., Sousa, A. M. M., Santpere, G., & Sestan, N.
- Affiliations
- Yale University (US)
- Universitat Pompeu Fabra (ES)
- Venue
- bioRxiv (Cold Spring Harbor Laboratory)
- Publisher
- openRxiv
- Published
- 2019-12-31
- OpenAlex
- W2997802861
- Cited by
- 7
- References
- 83
- Citations by year
- 2024: 1 · 2023: 2 · 2021: 3 · 2019: 1
- Type
- posted content
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Funders
- James S. McDonnell Foundation (MH116488, MH106874, MH110926, MH106934)
- Kavli Foundation (MH110926, MH106874, MH116488, MH106934)
- Fundación Bancaria Caixa d'Estalvis i Pensions de Barcelona (ID 100010434, 100010434)
- National Institutes of Health (ID 100010434, 100010434, MH116488, MH113257, MH106874)
- National Institute of Mental Health (R01MH110926, P50MH106934)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- retinoic acid signaling, prefrontal cortex development, mediodorsal thalamus, synaptogenesis, ALDH1A3, CYP26B1, RORB, retinoid X receptor gamma, retinoic acid receptor beta, cortical layer 4, motor cortex, human-macaque comparison, fetal brain development
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