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  • Review Article
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Cerebellar cortical organization: a one-map hypothesis

Nature Reviews Neuroscience volume 10, pages 670–681 (2009)Cite this article

Key Points

  • At least three different viewpoints have emerged of cerebellar cortical topography, based on the anatomy and physiology of climbing fibre inputs and Purkinje cell outputs, the physiology of mossy fibre inputs, restriction boundaries in gene expression and regional differences in Purkinje cell phenotype.

  • In this Review we consider some of the more commonly used terminology to describe cerebellar cortical organization with a view to providing some clarification. Overarching this, we argue the different terminologies are in fact unnecessary because both developmental and adult studies suggest that the different mapping techniques — anatomical, physiological and molecular — reveal different facets of a common topography.

  • The one-map hypothesis proposes that cerebellar architecture is built around an array of interdigitated transverse zones, each of which is subdivided into a series of rostrocaudally oriented Purkinje cell stripes, defined by the restricted expression of molecular markers, that are symmetrically distributed across the midline, highly reproducible between individuals, and conserved across species. The most comprehensively studied marker is zebrin II, which cloning studies revealed to be the metabolic enzyme aldolase C.

  • The molecular identity of each stripe may already be determined at the time the Purkinje cells become postmitotic, and, at the time a mouse is born, the molecular identity of individual Purkinje cells seems to be set and independent of cerebellar connectivity. The embryonic Purkinje cell clusters are the targets of the developing climbing fibre and mossy fibre afferents and, through this matching, the Purkinje cells form a template around which afferent topography is constructed.

  • Anatomical and physiological studies in adult animals have shown that climbing fibre afferents from different parts of the contralateral inferior olive form longitudinal zones within the cerebellar cortex. In some cases these zones can be subdivided into smaller units called microzones. Investigation of the relationship between longitudinal zones and Purkinje cell stripes has revealed extensive co-localization, consistent with the one-map hypothesis.

  • Anatomical studies have also found that mossy fibre terminal fields align with Purkinje cell stripes and also with climbing fibres associated with individual longitudinal zones, suggesting a common principle of organization.

  • By contrast, other studies support the notion that mossy fibres terminate as patches to form a fractured somatotopical map within the cerebellar cortex. The apparent discrepancy between stripes and patches may be explained by individual Purkinje cell stripes being subdivided into chains of small patches or microzones, which can be revealed by differential gene expression or electrophysiological mapping.

  • The one-map hypothesis therefore proposes that transverse zones are subdivided into stripes (one or more stripes equals a longitudinal zone); and stripes are further segmented longitudinally into microzones that correspond to one or more small patches.

  • The functional significance of this elaborate architecture remains to be determined but may be used for parallel processing of sensorimotor commands, energy efficient information processing, positional coding of sensory inputs and/or molecular fine-tuning of local circuits for specific functions such as motor learning.

Abstract

The fundamental architecture of the cerebellum is concealed within a terminological forest — transverse zones and stripes, longitudinal zones and microzones, patches, etc. To make things worse, the same term is used in different contexts to describe quite different patterns of spatial localization. Here we consider the possibility that this complexity hides the fact that the cerebellar cortex contains only one map, which has been charted in various ways.

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Figure 1: Gross morphology of the cerebellum.
Figure 2: Transverse zones and stripes.
Figure 3: The development of Purkinje cell stripes in mice.
Figure 4: Longitudinal zones.
Figure 5: Patches.
Figure 6: Patches can have similar spatial distributions as longitudinal zones and microzones.

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Acknowledgements

The authors thank J. Voogd and M. Usowicz for their comments on a draft manuscript and I. Sugihara for his comments on Table 2. The support of the BBSRC (R.A.), the Canadian Institutes of Health Research (R.H.) and the Wellcome Trust (R.A.) are gratefully acknowledged. Although space restrictions have meant it has only been possible to cite a small fraction of the relevant literature all mistakes and omissions are entirely Richard's fault.

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Authors and Affiliations

  1. Department of Physiology and Pharmacology, School of Medical Sciences, University of Bristol, Bristol, BS8 1TD, UK

    Richard Apps

  2. Department of Cell Biology & Anatomy, Hotchkiss Brain Institute, and Genes and Development Research Group, Faculty of Medicine, University of Calgary, Calgary, T2N 4N1, Alberta, Canada

    Richard Hawkes

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Supplementary information S1 (table)

The conservation of cerebellar zonal architecture (PDF 242 kb)

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Glossary

Inferior olivary complex

Collection of subnuclei located in the ventral medulla oblongata which are the sole source of climbing fibre afferents to the cerebellum.

Map

A systematic spatial representation of anatomical pathways, physiological activity and/or molecular features projected onto the cerebellar cortical surface.

Aldolase C

A brain-specific glycolytic isoenzyme that converts D-fructose 1,6-bisphosphate into glycerone phosphate and D-glyceraldehyde 3-phosphate.

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Apps, R., Hawkes, R. Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10, 670–681 (2009). https://doi.org/10.1038/nrn2698

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