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  • Review Article
  • Published:

Exuberance in the development of cortical networks

Nature Reviews Neuroscience volume 6, pages 955–965 (2005)Cite this article

Key Points

  • What is developmental exuberance? The exuberant development of neural circuits involves: the formation of long, transient axonal projections; the overproduction of short axonal branches and synapses, including polyinnervation and/or peaks of synaptic density; and the overproduction of dendritic branches and/or spines. In all cases, selection eventually leads to maintenance of some of the juvenile structures and elimination of others.

  • What function do exuberant structures have before their elimination? Some transient structures have important functions in constructing circuitry, but for others it is less clear whether the eliminated structures have important functions other than being substrates for the actions of selective mechanisms.

  • How general is the phenomenon? Development by exuberance is widespread during the formation of cerebral cortical circuits. It has been reported across different species and for different areas and projections, which suggests that it might have been a distinctive feature of mammalian development throughout evolution.

  • How are the projections eliminated? Two mechanisms can result in the elimination of the transient projections: neuronal death, or selective deletion of axons, axonal branches and/or synapses. The data available for the axonal pathways that interconnect cerebral cortical areas indicate a prevalent or exclusive role for the second mechanism.

  • What is the magnitude of elimination? The size of the elimination has been quantified for synapses and some long axonal tracts using electron microscopy. Less stringent quantification is available from experiments with axonal tracers. Studies show that some juvenile tracts are eliminated completely later in life.

  • Exuberant development of cortical connections occurs within boundaries established by the selective growth of axons from certain classes of neuron to specific targets, probably on the basis of selective molecular affinities. Once the axons have reached the proximity of their targets, selection occurs, particularly in the region of the cortical subplate.

  • The formation of the terminal axonal arbors in the targets is followed by continued exuberance and selection of axonal branches and synapses but within increasingly restricted topographical boundaries. The synaptic boutons are, from the onset, selectively distributed in the columnar and laminar dimensions, although their number exceeds that seen in adults.

  • Factors that control axonal selection include signals from the periphery (such as the retina), thyroid hormones, competition among axonal systems and/or between neurons for chemotrophic substances present in the target structure, and the expression of molecules that identify targets as appropriate to retain persistent innervation. This epigenetic control allows modification of the cortical networks in the light of changes in brain structure brought about by epigenetic or genetic changes.

  • The aetiology of neurological and psychiatric conditions such as dyslexia, attention deficit hyperactivity disorder and schizophrenia might involve abnormal growth and/or selection of cortical connections in the developing brain. Encouraging results for the study of cortical connectivity in the human brain have been provided by new developments in brain imaging and by tools for studying the dynamics of neuronal assemblies in the cerebral cortex.

Abstract

The cerebral cortex is the largest and most intricately connected part of the mammalian brain. Its size and complexity has increased during the course of evolution, allowing improvements in old functions and causing the emergence of new ones, such as language. This has expanded the behavioural and cognitive repertoire of different species and has determined their competitive success. To allow the relatively rapid emergence of large evolutionary changes in a structure of such importance and complexity, the mechanisms by which cortical circuitry develops must be flexible and yet robust against changes that could disrupt the normal functions of the networks.

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Figure 1: Exuberant projections into the corpus callosum from the visual areas of the cat.
Figure 2: Transient structures present during thalamocortical development.
Figure 3: Development of ipsilateral cortico-cortical connections from visual area 17 to area 18 in the cat.
Figure 4: Types of callosally projecting neuron in areas 17 and 18 of the cat visual cortex.
Figure 5: The growth of callosal axons into their site of termination is a multi-stage process.
Figure 6: Consequences of visual deprivation by bilateral eyelid suture on visual callosal axons originating near the area 17/18 border in the cat.

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Authors and Affiliations

  1. Department of Neuroscience, Karolinska Institutet, Retzius väg 8, Stockholm, S-17177

    Giorgio M. Innocenti

  2. Developmental Biology Laboratory, Biomedical Sciences, The University of Edinburgh, Hugh Robson Building, George Square, Edinburgh, EH8 9XD, UK

    David J. Price

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Correspondence to Giorgio M. Innocenti.

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DATABASES

Entrez Gene

BDNF

EMX2

FGF8

FOXG1

Id2

PAX6

Rzrβ

FURTHER INFORMATION

Genetic control of brain development

Price's laboratory

Glossary

TARGET

(of growing axons). The site, or structure, towards which an axon grows — ultimately one or more neurons.

OCULAR DOMINANCE

The neuronal property of responding preferentially to stimuli presented to one eye or the other.

TRACER

A tracer denotes a substance that is actively transported or diffuses along axons. Anterograde tracers move from neuronal cell bodies towards axon terminals, whereas retrograde tracers move from axon terminals (or damaged axons) towards neuronal cell bodies. Many tracers move in both directions.

TELENCEPHALON

One of the major components of the forebrain; thalamocortical axons grow through its ventral part to reach its dorsal part, where the cerebral cortex forms.

DIENCEPHALON

The component of the forebrain in which the thalamus develops.

PIONEER PROJECTIONS

(Or axons). Axons that precede the growth of others to a given target, and are thought to guide later-growing projections.

RECEPTIVE FIELD

A region in the periphery that, when stimulated in an appropriate way, produces a response in a particular sensory neuron.

GROWTH CONE

A highly dynamic structure at the growing end of an axon (or dendrite) that steers axonal (or dendritic) growth by decoding cues in the environment.

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Innocenti, G., Price, D. Exuberance in the development of cortical networks. Nat Rev Neurosci 6, 955–965 (2005). https://doi.org/10.1038/nrn1790

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