Abstract
It is often thought that the construction of cortical circuits occurs as the result of an elegantly designed process that unfolds sequentially as an animal develops until adult functional networks emerge. In reality, cortical circuits are shaped by evolutionary mechanisms, changes in developmental programmes driven by neuronal activity or epigenetic mechanisms and the need to adapt to the external world, and must pass through several important phases and timely checkpoints as they form. Some cortical cell types serve multiple functions during this developmental journey and are then reused (or ‘recycled’) to perform different functions in the adult cortex. Understanding the different stages of the cortical construction process and taking into account the ways in which cellular functions change across time and space is therefore essential if we are to build a comprehensive framework of cortical wiring in both health and disease.
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Acknowledgements
The authors thank M. Thion as well as all the members of their laboratories for constructive comments. This work was supported by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 646925) and by the Fondation Bettencourt Schueller to R.C. and by the ANR iReelax and Microsenso (grant agreements no. 198187 and no. 198184), and the FRM Équipe and the Cercle FSER laureate programmes to S.G. R.C. is supported by CNRS, S.G. is a member of the ENP programme.
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Glossary
- Cajal–Retzius cells
-
Early born guidepost neurons located in the marginal zone that are largely eliminated in the postnatal cortex and maintained in the hippocampus.
- Subplate cells
-
Early born guidepost neurons located deep the cortical plate that are largely eliminated in the postnatal cortex.
- Ventricular zones
-
The proliferative zones lining the ventricular surface.
- Ganglionic eminences
-
Transitory structures in the development of the forebrain that are the site of genesis of most GABAergic cortical neurons.
- Cortical plate
-
The transient developmental structure formed in corticogenesis, which includes cortical layers 2–6.
- Synaptic pruning
-
The elimination of supernumerary synapses during development.
- Gap junction
-
A type of cellular junction in which adjacent cells are connected through protein channels, making them chemically or electrically coupled.
- Proto-ensembles
-
The first groups of co-active neurons from which other ensembles develop.
- Developmental apoptosis
-
Programmed cell death during development.
- Outer subventricular zone
-
A proliferative zone located far from the ventricular zone, which contains basal progenitors and is found in ferrets and primates but not in mice.
- Basal progenitors
-
Progenitors located in the outer subventricular zone.
- Intermediate progenitors
-
Progenitors located in the subventricular zone that are present in all mammalian species.
- Hub cells
-
Neurons displaying an exceptional output connectivity that can influence network dynamics.
- Pioneer neurons
-
Neurons born at the earliest time points of neurogenesis.
- Critical period
-
The developmental period of experience-dependent refinement of cortical circuits.
- Perineuronal nets
-
Extracellular matrix structures supporting synapse stabilization.
- Neuronal ensemble
-
A group of co-active neurons.
- Sparsification
-
The developmental process by which activity shifts from highly correlated to sparse.
- Active exploration
-
Self-initiated examination of the external world.
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Cossart, R., Garel, S. Step by step: cells with multiple functions in cortical circuit assembly. Nat Rev Neurosci 23, 395–410 (2022). https://doi.org/10.1038/s41583-022-00585-6
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DOI: https://doi.org/10.1038/s41583-022-00585-6
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