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Encoding asymmetry within neural circuits

Key Points

  • Asymmetries between the left and right sides of the nervous system are present throughout the animal kingdom, from invertebrates to mammals.

  • There are two fundamentally distinct ways in which neural circuits can be lateralized: one involves specification of common components on both sides, but to different extents. The other involves unilateral structures, which are present exclusively on one side.

  • Both environmental and genetic factors contribute to the development of neural asymmetries. Research in model organisms is beginning to reveal the molecular-genetic pathways that control the development of brain lateralization.

  • Theoretical advantages of brain asymmetry include the capacity for parallel processing, the specialization of left and right sides for distinct computations and the restriction of information processing within local circuits characterized by short, fast axonal connections. However, at present we do not understand the specific functions of the majority of known circuit asymmetries.

  • Recent technological advances that allow neural activity to be measured and manipulated during behaviour have enormous potential to reveal the functions of asymmetric circuits. Furthermore, large-scale projects that are defining brain anatomy and connectivity in unprecedented detail will help to reveal the circuit organization responsible for functional and behavioural lateralization.

Abstract

Genetic and environmental factors control morphological and functional differences between the two sides of the nervous system. Neural asymmetries are proposed to have important roles in circuit physiology, cognition and species-specific behaviours. We propose two fundamentally different mechanisms for encoding left–right asymmetry in neural circuits. In the first, asymmetric circuits share common components; in the second, there are unique unilateral structures. Research in both vertebrates and invertebrates is helping to reveal the mechanisms underlying the development of neural lateralization, but less is known about the function of circuit asymmetries. Technical advances in the coming years are likely to revolutionize our understanding of left–right asymmetry in the nervous system.

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Figure 1: Classes of asymmetric neural circuitry.
Figure 2: Light-induced visual lateralization in birds.
Figure 3: Circuit asymmetries associated with the zebrafish epithalamus.
Figure 4: Sensory asymmetries and the computation of chemotaxis in worms.

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Acknowledgements

We thank members of our laboratories, colleagues, R. Poole and the referees for discussions and comments on the manuscript, and K. Palma for help in drawing the figures. Our work on this topic is supported by the Wellcome Trust (I.H.B. and S.W.W.), the Howard Hughes Medical Institute (M.L.C.), Fondecyt (1090242, 1120558: M.L.C.) and the Millennium Science Initiative (P09-015-F: M.L.C.).

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Correspondence to Miguel L. Concha, Isaac H. Bianco or Stephen W. Wilson.

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Glossary

Bilateria

Animals showing bilateral symmetry: that is, having left and right sides defined by their anterior to posterior (head to tail) and dorsal to ventral (back to front) axes.

Ontogeny

The development of the animal from fertilized egg to maturity.

Thalamofugal

The thalamofugal pathway is a set of central visual pathways in birds that is equivalent to the mammalian geniculocortical pathway.

Tectofugal pathway

A set of central visual pathways in birds that is equivalent to the extrageniculocortical pathway of mammals.

Arcuate fasciculus

A tract linking the language association areas of Broca and Wernicke.

Corpus callosum

The major commissural pathway that connects the left and right hemispheres.

Antisymmetry

Equal frequency of left and right sidedness of the asymmetry within the population.

Directional asymmetry

A predominant sidedness to the asymmetry within the population.

Visual hyperpallium

A region (along with the entopallium) of the bird telencephalon that is involved in visual processing of information from the tectofugal and thalamofugal pathways, respectively.

Precocial

Species in which the young are relatively mature and mobile from the moment of birth or hatching.

Altricial

Species in which the young are highly dependent from the moment of birth or hatching

Functional MRI

Functional MRI detects changes in blood flow that correlate with intensity of neuronal activity, providing a technique for assessing which brain areas are active during particular cognitive or other activities.

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Concha, M., Bianco, I. & Wilson, S. Encoding asymmetry within neural circuits. Nat Rev Neurosci 13, 832–843 (2012). https://doi.org/10.1038/nrn3371

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