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The Journal of Neuroscience, November 15, 2006, 26(46):12067-12080; doi:10.1523/JNEUROSCI.2905-06.2006

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Behavioral/Systems/Cognitive
Precise Spatial Relationships between Mossy Fibers and Climbing Fibers in Rat Cerebellar Cortical Zones

Angelique Pijpers,¹ Richard Apps,^2 * Joanne Pardoe,² Jan Voogd,¹ and Tom J. H. Ruigrok^1 *

¹Department of Neuroscience, Erasmus Medical Center Rotterdam, 3000 DR Rotterdam, The Netherlands, and ²Department of Physiology, University of Bristol, BS8 1TD Bristol, United Kingdom

Correspondence should be addressed to Tom J. H. Ruigrok, Department of Neuroscience, Erasmus Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands. Email: t.ruigrok{at}erasmusmc.nl

Classically, mossy fiber and climbing fiber terminals are regarded as having very different spatial distributions in the cerebellar cortex. However, previous anatomical studies have not studied these two major cerebellar inputs with sufficient resolution to confirm this assumption. Here, we examine the detailed pattern of collateralization of both types of cerebellar afferent using small injections of the bidirectional tracer cholera toxin b subunit into the posterior cerebellum. The cortical and zonal location of these injections was characterized by mapping climbing fiber field potentials, the distribution of retrogradely labeled olivary neurons, and the intrinsic zebrin pattern of Purkinje cells.

Labeled climbing fiber collaterals were distributed as longitudinal strips and were always accompanied by clusters of labeled mossy fiber rosettes in the subjacent granular layer. Two- and three-dimensional reconstructions and quantitative analysis showed that mossy fibers also collateralized to other stripe-like regions usually below Purkinje cells with the same zebrin-positive or zebrin-negative characteristics as that of the injection site and associated climbing fiber collaterals. The distribution of retrogradely labeled neurons in two major sources of mossy fibers, the lateral reticular and basilar pontine nuclei, revealed interlobular and some interzonal differences.

These data indicate that nonadjacent cerebellar zones, sharing the same climbing fiber input and zebrin identity, also share a common mossy fiber input. Other cerebellar cortical regions that receive collaterals from the same mossy fibers usually also have the same zebrin signature. Together with the distribution of neurons in precerebellar centers, the findings suggest a revision of the modular hypothesis for information processing in the cerebellar cortex.

Key words: Purkinje cell; inferior olive; zebrin; cerebellar modules; mossy fiber rosette; cholera toxin b subunit

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Received Nov. 18, 2005; revised Sept. 27, 2006; accepted Oct. 13, 2006.

Correspondence should be addressed to Tom J. H. Ruigrok, Department of Neuroscience, Erasmus Medical Center Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands. Email: t.ruigrok{at}erasmusmc.nl

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