*Department of Physiology,
Anatomy & Genetics,
University of Oxford, Oxford,
OX1 3PT, UK.
||
Department of
Morphology, Institute of
Experimental Medicine, St
Petersburg, 197376, Russia.
§
Department of Neurobiology
and Kavli Institute of
Neuroscience, Yale University
Medical School, New Haven,
Connecticut 208001, USA.
Correspondence to P.R. & I.B.
e-mails:
pasko.rakic@yale.edu; irina.
bystron@dpag.ox.ac.uk
doi:10.1038/nrn2252
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.
Development of the human cerebral
cortex: Boulder Committee revisited
Irina Bystron*
||
, Colin Blakemore* and Pasko Rakic
§
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.
The mammalian cerebral cortex is a complex laminated
structure that contains a bewildering diversity of neurons
and has rich local and extrinsic connectivity. Regional
variations in cytoarchitecture are superimposed on a
common plan of layers, cell types and connections
1
.
The explosion in the size of the cerebral hemispheres
during mammalian evolution is correlated with increas-
ing behavioural and cognitive capacity. The enormous
human cortex underpins our perception, memories,
thoughts and language.
In all mammals, the neocortex forms at the outer surface
of the embryonic cerebral vesicle, at the rostral end of the
neural tube, through the migration of neurons from pro-
liferative regions near the cerebral ventricle
2,3
. The arrival
of migrating neurons establishes laminar compartments,
some of which change or even disappear during develop-
ment. The sequence of events that take place during corti-
cal development, as it was then understood, was described
more than 35 years ago by the Boulder Committee
4
. This
committee, meeting in Boulder, Colorado, was con-
vened by the American Association of Anatomists, the
main forum for the growing fields of neuroanatomy and
embryology. The committee’s remit was to standardize
the heterogeneous and confusing nomenclature for the
developing vertebrate CNS that had emerged from
the blossoming of knowledge. Richard Sidman presented
diagrams of embryonic cortical development (FIG. 1A), based
on the observations of P.R., then an assistant professor
in his department. The committee’s report stated:
The layers and cells of the early developing
central nervous system lack direct counterparts
in the adult and must be designated by a special
terminology. The inconsistent and inaccurate
language now in use leads to misunderstanding
and a revision is proposed in which the four
fundamental zones are termed the ventricular,
subventricular, intermediate, and marginal zones.
Each is defined according to the form, behaviour,
and fate of its constituent cells. All neurons and
macroglia of the central nervous system can be
derived from these developmental zones.
Thus, the committee recommended names for each
of the transient embryonic cellular compartments (or
‘zones’) and gave their interpretation of the major devel-
opmental events. This model has been widely adopted
as a generic description of the development of the entire
vertebrate CNS.
In the past three decades, experimental studies on
normal and genetically altered rodents have driven the
analysis of cortical development. This has given us new
insights into the regulation of cell division and pro-
grammed cell death, which determine neuron number
5,6
,
and the mechanisms of neuronal migration
3,7,8
. Patterns
of genetic expression are being elucidated, including the
expression of transcription factors that are thought to
influence regional differentiation and regulate broad
aspects of mitotic activity, fate determination and dif-
ferentiation
9–12
. Recent studies have revealed new types
of transient neurons and proliferative cells outside the
classical neuroepithelium, new routes of cellular migration
and additional cellular compartments
13–18
. Furthermore,
we know much more about intrinsic connectivity and
the formation of axonal projections into and out of the
cortex
19–21
. Thus, our understanding of the timing and
sequence of developmental events in the cerebral wall
has changed radically since the work of the Boulder
Committee.
Despite the march of knowledge, the Boulder
Committee’s nomenclature continues to be widely used.
Their summary diagram (FIG. 1A) has been reproduced,
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