Systematic analysis of neuronal wiring of the rodent deep cerebellar nuclei reveals differences reflecting adaptations at the neuronal circuit and internuclear levels

Abstract

A common view of the architecture of different brain regions is that, despite their heterogeneity, they have optimized their wiring schemes to make maximal use of space. Based on experimental findings, computational models have delineated how about two-thirds of the neuropil is filled out with dendrites and axons optimizing cable costs and conduction time while keeping the connectivity at the highest level. However, whether this assumption can be generalized to all brain regions has not yet been tested. Here we quantified and charted the components of the neuropil in the four deep cerebellar nuclei (DCN) of the rat's brain. We segmented and traced the neuropil stained with one of two antibodies, one antibody against dendritic microtubule-associated proteins (MAP2a,b) and the second against the Purkinje cell axons (PCP2). We compared fiber length density, average fiber diameter, and volume fraction within different components of the DCN in a random, systematic fashion. We observed differences in dendritic and axonal fiber length density, average fiber diameters, and volume fraction within the four different nuclei that make up the DCN. We observe a relative increase in the length density of dendrites and Purkinje cell axons in two of the DCN, namely, the posterior interposed nucleus and the lateral nucleus. Furthermore, the DCN have a surprisingly low volume fraction of their dendritic length density, which we propose is related to their special circuitry. In summary, our results show previously unappreciated functional adaptations among these nuclei.

Keywords: 3D reconstructions; Purkinje cells; cerebellar nuclei; motor systems; quantitative immunohistochemistry; wiring schemes.