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  • Review Article
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Left–right asymmetry in the nervous system: the Caenorhabditis elegans model

Nature Reviews Neuroscience volume 3, pages 629–640 (2002)Cite this article

Key Points

  • The body plan of most adult animals is largely bilaterally symmetrical, although several organs, such as the heart, liver and spleen, are only present on one side of the animal. In a second type of asymmetry, structures that are present on both sides of the body show deviations from bilateral symmetry. In vertebrates, this symmetry breakage is manifested in the asymmetrical size of otherwise bilaterally symmetrical structures. In invertebrates, it is apparent at the level of gene expression patterns and cell positioning.

  • Two-thirds of the neurons of the nematode Caenorhabditis elegans are present as bilaterally symmetrical pairs, and most of the remaining neurons are located on or close to the midline, with no contralateral analogue. Within the head ganglia, there are four neurons that are located on only one side of the animal; these are termed 'unilateral' neurons. Bilateral symmetry in the ventral nerve cord (VNC) is more subtle, and the left and right fascicles of the VNC are the only major fascicles in the worm that are not strictly bilaterally symmetrical.

  • Similar lineage histories are neither sufficient nor necessary for two cells to adopt bilaterally symmetrical cell fates. The adoption of bilateral symmetry by two neurons that have no lineage relationship requires extensive rearrangements of cell position; in some cases, neuroblasts even migrate over the midline to take up a bilaterally symmetrical position to their analogous cell.

  • Particularly intriguing components of left–right (L–R) asymmetry in the C. elegans nervous system are neuron pairs that are bilaterally symmetrical in terms of several criteria, but, after bilaterality has been established, undergo L–R-specific sub-differentiation programmes. Examples include the AWC odorsensory neurons, the ASE taste receptor neurons and the Q blast cells.

  • Breakage of bilateral symmetry has also been observed in the nervous systems of several other invertebrate and vertebrate species. In the leech, two classes of neurons within the ganglia of each segment undergo L–R asymmetrical sub-differentiation programmes. In the human brain, there are significant size differences in the temporal lobes of the left and right hemispheres. The zebrafish brain shows L–R asymmetry in the size of the habenular nuclei, and the parapineal organ is located on the left side of the midline.

  • The progression from symmetry to antisymmetry (randomized asymmetry) to directional asymmetry can be observed both ontogenetically and phylogenetically. The creation of a symmetrical body axis could have resulted in redundancy in L–R structures, providing evolution with the 'playground' to diversify along the L–R axis; for example, leading to the diversification of sensory function in C. elegans.

Abstract

Although the overall architecture of the nervous system of most animals shows a large degree of bilateral symmetry, there are striking patterns of left–right (L–R) asymmetry in the brains of some species. Some structures show L–R-specific differences in size, whereas others show asymmetrical patterns of gene expression and have diversified at the functional level. The nematode Caenorhabditis elegans offers a unique opportunity to address how symmetrical neuronal assemblies deviate to create functional lateralizations. Here, we provide a detailed cellular and molecular perspective on L–R asymmetry in the nervous system of C. elegans. We also give an overview of symmetry and asymmetry in the nervous systems of other organisms. We will relate these observations to general concepts of the mechanistic and phylogenetic origin of laterality.

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Figure 1: Left–right symmetry of neuronal nuclei position, axon fascicle position and axon placement within fascicles.
Figure 2: Left–right symmetry of axon fascicle position and axon placement within fascicles.
Figure 3: Lineage descent of bilaterally symmetrical cells.
Figure 4: Breaking left–right symmetry in the AWCL/AWCR, ASEL/ASER, QL/QR and P11/P12 neurons.
Figure 5: Examples of symmetry and asymmetry in other invertebrates and in vertebrates.
Figure 6: Progression from symmetry to antisymmetry to directional asymmetry can be observed ontogenetically as well as phylogenetically.
Figure 7: A model for the induction of left–right asymmetry in the Caenorhabditis elegans nervous system.

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Acknowledgements

We thank H. Bigelow for help with evaluating asymmetry at the level of synaptic connectivity, and C. Kenyon, A. Schier, B. Wood and P. Sengupta for comments on the manuscript. Research in our lab is supported by the Whitehall, March of Dimes and McKnight Foundations, the American Paralysis Association, the Muscle Dystrophy Association and the National Institutes of Health (NIH). O.H. is a Searle and Sloan scholar. R.J.J. is supported by a National Science Foundation predoctoral fellowship, and S.C. by an NIH predoctoral fellowship.

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  1. Department of Biochemistry and Molecular Biophysics, Center for Neurobiology and Behavior, Columbia University, College of Physicians and Surgeons, New York, 10032, New York, USA

    Oliver Hobert, Robert J. Johnston Jr & Sarah Chang

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  1. Oliver Hobert
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Correspondence to Oliver Hobert.

Supplementary information

41583_2002_BFnrn897_MOESM1_ESM.pdf

Left–right symmetry of axon fascicle position in the ventral ganglion. The image is based on an electron micrograph from which the outlines of the axon cross-sections (lower half, coded by shading) and cell bodies (upper half, not colour coded) have been traced. The electron micrograph was obtained from a transverse section through Caenorhabditis elegans12. The approximate location of the section is shown in FIG. 2a. Color coding: red, left–right (L–R) asymmetrical neuron; beige, L–R symmetrical pairs (matched by shading). Note that as well as similar cell positions (FIG. 1b), L–R bilaterally homologous neurons also share a similar axonal neighbourhood. (PDF 136 kb)

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DATABASES

LocusLink

lefty1

nodal-related

pitx2

WormBase

AB praaa

AIYL

AIYR

ALA

AQR

ASEL

ASER

AVAL

AVAR

AVDL

AVDR

AVEL

AVER

AVG

AVL

AVM

AWBL

AWBR

AWCL

AWCR

dpy-19

EGL-20

gcy-5

gcy-6

gcy-7

lim-6

lin-12

mab-5

nid-1

P1

P2

P11

P12

PQR

PVM

QL

QR

RID

RIH

RIR

RIS

RMED

RMEV

SABD

SDQL

SDQR

str-2

unc-40

UNC-6

Y

FURTHER INFORMATION

Encyclopedia of Life Sciences

Caenorhabditis elegans as an experimental organism

Caenorhabditis elegans embryo: establishment of asymmetry

vertebrate embryo: establishment of left–right asymmetry

Flybrain

Flybrain

The Hobert Lab

The Hobert Lab

Glossary

NEMATODE

A phylum of worms that are characterized by cylindrical, unsegmented bodies.

VENTRAL NERVE CORD

A major bundle of axons that runs along the ventral side of the animal. It contains mainly motor neuron axons and some interneuron axons, and is probably homologous to the vertebrate spinal cord.

CHEMOTAXIS

Directed movement of an animal towards or away from a point source of a chemical cue. If the cue is a volatile odour, the process is known as 'odortaxis'; if the cue is water soluble, the process is known as 'chemotaxis'.

MOSAIC ANALYSIS

A method that is used to determine in what cell type an individual gene product acts. In C. elegans, the method is based on the random loss of extrachromosomal pieces of DNA that contain the gene of interest. Loss or presence of the DNA is correlated with the absence or presence of the mutant phenotype, allowing the cell type in which the gene acts to be inferred.

HOMEOBOX GENES

Homeobox genes are transcription factors that contain a homeodomain, which binds directly to DNA. Some homeobox genes are organized in chromosomal clusters (for example, HOX cluster genes) and are involved in determining regional identity along the anteroposterior axis. Non-HOX-cluster homeobox genes act in a variety of locations during development.

HYPODERMAL RIDGE

A ridge of hypodermal (equivalent to epidermal) tissue that is located between the left and right fascicles of the ventral nerve cord. Structurally and functionally, it is thought to be similar to midline glial cells in the fly and in vertebrates.

GASTRULATION

The process by which the embryo becomes regionalized into three layers: ectoderm, mesoderm and endoderm.

TELEOSTS

A taxonomic group that includes most bony fish, notable exceptions being sturgeons and lungfish.

PARAPINEAL ORGAN

A photoreceptive structure in the forebrain that forms a complex with the pineal organ.

PINEAL ORGAN

A photoreceptive organ that is an important component of the circadian clock in lower vertebrates.

MONOCILIA

Cilia are present on the outside of many embryonic tissues. They are thin, motile processes that extend into the extraembryonic space. Monocilia are an ultrastructurally specialized type of cilia that are found, for example, on node cells.

NODE

A major organizing centre in primitive-streak-stage embryos that regulates pattern formation. It is known as Hensen's node in chick and the Spemann organizer in frog.

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Hobert, O., Johnston, R. & Chang, S. Left–right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat Rev Neurosci 3, 629–640 (2002). https://doi.org/10.1038/nrn897

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