Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkey

Piotr Majka,Piotr Majka,Piotr Majka,Piotr Majka,Piotr Majka,Sylwia Bednarek,Sylwia Bednarek,Panagiota Theodoni,Panagiota Theodoni,Panagiota Theodoni,David H Reser,Natalia Jermakow,Natalia Jermakow,Lauretta Passarelli,Partha P Mitra,Sophia Bakola,David H Reser,Sophia Bakola,Shi Bai,Marcello G P Rosa,Marcello G P Rosa,Marcello G P Rosa,Sophia Bakola,Sophia Bakola,Daniel K Wójcik,Daniel K Wójcik,Katrina H Worthy,Katrina H Worthy,Jonathan M Chan,Jonathan M Chan,Jonathan M Chan,Xiao-Jing Wang,David H Reser

doi:10.1038/s41467-020-14858-0

Abstract

Understanding the principles of neuronal connectivity requires tools for efficient quantification and visualization of large datasets. The primate cortex is particularly challenging due to its complex mosaic of areas, which in many cases lack clear boundaries. Here, we introduce a resource that allows exploration of results of 143 retrograde tracer injections in the marmoset neocortex. Data obtained in different animals are registered to a common stereotaxic space using an algorithm guided by expert delineation of histological borders, allowing accurate assignment of connections to areas despite interindividual variability. The resource incorporates tools for analyses relative to cytoarchitectural areas, including statistical properties such as the fraction of labeled neurons and the percentage of supragranular neurons. It also provides purely spatial (parcellation-free) data, based on the stereotaxic coordinates of 2 million labeled neurons. This resource helps bridge the gap between high-density cellular connectivity studies in rodents and imaging-based analyses of human brains.

Highlights

Understanding the principles of neuronal connectivity requires tools for efficient quantification and visualization of large datasets
Complete maps of neuronal connections have been achieved for simple nervous systems3, but uncovering the organizational principles that govern neuronal connectivity in mammals is most realistically tackled at the mesoscopic level4, by taking advantage of regularities in the patterns of connections formed by clusters of adjacent neurons5
The Marmoset Brain Connectivity Atlas is accessible through the http://marmosetbrain.org portal. This resource provides online access to the primary experimental data, as well as the database of connectivity patterns quantified according to the parcellation of the marmoset cortex29

Summary

Introduction

Understanding the principles of neuronal connectivity requires tools for efficient quantification and visualization of large datasets. The present release incorporates methodological refinements which improve the accuracy of the attribution of neurons to areas, as well as new datasets including the stereotaxic coordinates of neurons revealed by the experiments, estimates of the white matter distances involved in each connection, and volumetric representations that enable integration with neuroimaging platforms This functionality is made available through a dedicated analysis interface which enables quantification and visualization of results in individual cases, or aggregated by cortical area. The most extensive resources on cortical connections in nonhuman primates currently available are CoCoMac (an online platform based on meta-analysis of the literature) and CoreNets (a collection of tracer injections in 29 areas, obtained with consistent methodology)15,16 Both of these give access to information on the macaque monkey cortex, but are limited in terms of access to full datasets and integrated functionality for analysis. Marmosets are small (~350 g) New World primates which have become increasingly important for studies of cognitive function and dysfunction, in part due to the relatively short developmental cycle, which facilitates the development of transgenic lines and studies across the life span

Methods

Results

Conclusion