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  • Review Article
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Development of the human cerebral cortex: Boulder Committee revisited

Nature Reviews Neuroscience volume 9, pages 110–122 (2008)Cite this article

Key Points

  • Much more is now known about human cortical development than was known in 1970, when the Boulder Committee attempted to standardize the heterogeneous and confusing nomenclature that was used in the field. In light of this, a revised standardization is needed.

  • A transient layer with a diverse population of neurons forms between the neuroepithelium and the pial surface of the dorsal telencephalon before the appearance of the cortical plate (CP). The term preplate, which is already widely used, should be adopted for this layer.

  • The subventricular zone appears as a distinctive proliferative layer before the emergence of the CP, earlier than previously recognized.

  • There is no distinct cell-sparse layer under the pial surface before the CP forms. Thus, the term marginal zone should be used only after the appearance of the CP, to refer to the residual superficial part of the preplate, which becomes the layer 1 of the mature cortex.

  • The term intermediate zone (IZ) has been used in various ways. In future it should be reserved for the heterogeneous compartment that lies between the proliferative layers and the postmigratory cells above. The IZ contains radially and tangentially migrating cells and a thickening layer of extrinsic axons that eventually constitutes the white matter.

  • The subplate (SP) is a distinct and functionally important transient layer, located directly below the cortical plate, which was not recognized by the Boulder Committee. In rodents and carnivores most SP neurons are born before the first CP cells. In humans, preplate cells also contribute to the SP, but its substantial thickening at later stages probably involves the addition of later-born neurons.

Abstract

In 1970 the Boulder Committee described the basic principles of the development of the CNS, derived from observations on the human embryonic cerebrum. Since then, numerous studies have significantly advanced our knowledge of the timing, sequence and complexity of developmental events, and revealed important inter-species differences. We review current data on the development of the human cerebral cortex and update the classical model of how the structure that makes us human is formed.

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Figure 1: The Boulder Committee's 1970 schematic model of human neocortical development, and a proposed revision.
Figure 2: Early formation of layers in the embryonic human ventrolateral cerebral wall.
Figure 3: Subcompartmentalization within the cortical wall.
Figure 4: Human cerebral wall at GW12.
Figure 5: Morphology and origin of Cajal–Retzius cells.

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Acknowledgements

We are grateful to J. Rubenstein, R. Hevner, D. D. M. O'Leary, S. Lindsay and F. Guillemot for discussion about the IZ and the SP. This work was supported by the Kavli Institute for Neuroscience at Yale (P.R. & I.B.), the National Institute of Neurological Disorders and Stroke of the US Public Health Service (P.R.) and the Hill Foundation (I.B.)

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Authors and Affiliations

  1. Department of Physiology, Anatomy & Genetics, University of Oxford, Oxford, OX1 3PT, UK

    Irina Bystron & Colin Blakemore

  2. Department of Morphology, Institute of Experimental Medicine, St Petersburg, 197376, Russia

    Irina Bystron

  3. Department of Neurobiology and Kavli Institute of Neuroscience, Yale University Medical School, New Haven, 208001, Connecticut, USA

    Pasko Rakic

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Glossary

Neocortex

The evolutionarily newest portion of the cerebral cortex. It is particularly enlarged in primates and underpins higher mental functions for humans.

Neuroepithelium

A layer of proliferating neuroepithelial cells that makes up the neural plate and neural tube.

Neural plate

The neuroectodermal epithelium before the neural groove and neural tube form.

Interkinetic nuclear movement

The apical-basal-apical migration of the neuroepithelial cell nucleus during the cell cycle.

Predecessor cell

A type of neuron that arrives beneath the pial surface of the human embryonic forebrain before the neural tube has even finished closing. Predecessor cells appear in the developing cortex before any other post-mitotic cells.

Golgi staining

A staining technique introduced by Camillo Golgi in 1873 that selectively stains neurons with silver nitrate.

Projection neuron

A type of glutamatergic neuron, characterized by a typical pyramidal morphology, that extends its axon to distant intracortical, subcortical or subcerebral targets. Projection neurons are born in the VZ, and their lineage is different from that of the interneurons.

Interneurons

A heterogeneous group of non-pyramidal, mostly GABAergic neurons that project locally and appear to be mainly inhibitory. In rodents most interneurons originate in the ganglionic eminence of the ventral forebrain and then migrate tangentially to the neocortex, whereas in humans and non-human primates they originate from both the ganglionic eminence and the SVZ of the dorsal telencephalon. In the human brain there might be pronounced differences in the proportions of neurons from the two sources.

Corticofugal axon

An axon that originates from a cortical neuron but projects ouside the cortex to subcortical structures.

Internal capsule

A large bundle of axons that reciprocally connects the cortex with the subcortical structures of the brain.

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Bystron, I., Blakemore, C. & Rakic, P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9, 110–122 (2008). https://doi.org/10.1038/nrn2252

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