Uncovering specific changes in network wiring underlying the primate cerebrotype

Abstract

Regular scaling of brain networks during evolution has been proposed to be the major process leading to enlarged brains. Alternative views, however, suggest that deviations from regular scaling were crucial to the evolution of the primate brain and the emergence of different cerebrotypes. Here, we examined the scaling within the major link between the cerebellum and the cerebral cortex by studying the deep cerebellar nuclei (DCN). We compared the major axonal and dendritic wiring in the DCN of rodents and monkeys in search of regular scaling. We were able to confirm regular scaling within the density of neurons, the general dendritic length per neuron and the Purkinje cell axon length. However, we also observed specific modification of the scaling rules within the primates’ largest and phylogenetically newest DCN, the dentate nucleus (LN/dentate). Our analysis shows a deviation from regular scaling in the predicted dendritic length per neuron in the LN/dentate. This reduction in the dendritic length is also associated with a smaller dendritic region-of-influence of these neurons. We also detected specific changes in the dendritic diameter distribution, supporting the theory that there is a shift in the neuronal population of the LN/dentate towards neurons that exhibit spatially restricted, clustered branching trees. The smaller dendritic fields would enable a larger number of network modules to be accommodated in the primate LN/dentate and would provide an explanation for the unique folded structure of the primate LN/dentate. Our results show that, in some brain regions, connectivity maximization (i.e., an increase of dendritic fields) is not the sole optimum and that increases in the number of network modules may be important for the emergence of a divergent primate cerebrotype.Electronic supplementary materialThe online version of this article (doi:10.1007/s00429-017-1402-6) contains supplementary material, which is available to authorized users.

Quantitative organization of the excitatory synapses of the primate cerebellar nuclei: further evidence for a specialized architecture underlying the primate cerebellum

“…A further new finding of our study is that there is a lower number of vGluT1+ excitatory synapses per neuron in the LN/dentate of the rhesus monkey compared to the rat’s LN/dentate. This result tallies well with the lower dendritic length per neuron that we already reported in the monkey LN/dentate (Hamodeh et al 2017) and lends further support to our model of hyposcalled dendrites that underlie the special architecture of the LN/dentate. The hyposcaled dendritic arbors (Hamodeh et al 2017) and vGluT1+ inputs (this study) could allow for an increase in the number of independent/segregated parasagittal strips in the cerebellar hemispheres connected to the LN/dentate, which would confirm a recent prediction (Jorntell 2017).…”

“…This result is in agreement with our previous observation finding similar differences in the rat vGluT1 densities (Mao et al 2018). This result also confirms that our observation of variation in the dendritic length density in the macaque DCN (Hamodeh et al 2014, 2017) is accompanied by similar vGluT1 variations, i.e., regions with higher dendritic length densities show higher vGluT1+ densities. In addition, our results also point to some important differences between the rat and monkey LN/dentate, also confirming our previous dendritic quantifications showing hyposcalled dendrites in the LN/dentate.…”

“…We calculated the mean bouton number per DCN neuron on the basis of our vGluT1 and vGluT2 labelled boutons in the current study and the neuron density in our previous study (Hamodeh et al 2014, 2017). The vGluT1 and 2 bouton number per neuron is similar in rat and monkey.…”

“…This is comparable to the reduction in neuronal density (8640 vs. 25,300) to 34% of the rat densities and shows that the overall vGluT1 synapses per neuron remain comparable. A comparison of the dendritic length density (Hamodeh et al 2017) of monkeys vs. rats (51.5 vs. 39.8 m/mm 3 ), shows a lower reduction to 77% of the rat values and would point to a general reduction in the number of vGluT synapses per dendritic length. Excitatory synapses to the DCN neurons largely originate from the precerebellar nuclei.…”

“…In fact a different prediction emerges if we look at the wiring components within the DCN. In a previous study (Hamodeh et al 2017), we quantified and compared the wiring components between the rat and rhesus monkey DCN. We found that although the dendritic length density (dendritic length per tissue volume) was increased within the LN/dentate, a different picture emerged when we compared the dendritic length per neuron (dendritic length density normalized by neuron density).…”