Elsevier

NeuroImage

Volume 45, Issue 1, March 2009, Pages 52-59
NeuroImage

A population-average MRI-based atlas collection of the rhesus macaque

https://doi.org/10.1016/j.neuroimage.2008.10.058Get rights and content

Abstract

Magnetic resonance imaging (MRI) studies of non-human primates are becoming increasingly common; however, the well-developed voxel-based methodologies used in human studies are not readily applied to non-human primates. In the present study, we create a population-average MRI-based atlas collection for the rhesus macaque (Macaca mulatta) that can be used with common brain mapping packages such as SPM or FSL. In addition to creating a publicly available T1-weighted atlas (http://www.brainmap.wisc.edu/monkey.html), probabilistic tissue classification maps and T2-weighted atlases were also created. Theses atlases are aligned to the MRI volume from the Saleem, K.S. and Logothetis, N.K. (2006) atlas providing an explicit link to histological sections. Additionally, we have created a transform to integrate these atlases with the F99 surface-based atlas in CARET. It is anticipated that these tools will help facilitate voxel-based imaging methodologies in non-human primate species, which in turn may increase our understanding of brain function, development, and evolution.

Introduction

Functional and structural neuroimaging research studies in humans have benefited greatly from rapidly maturing computational neuroanatomical methods that enable multi-subject voxel-wise approaches (Ashburner and Friston, 2000, Friston et al., 1999a, Friston et al., 1999b, Woods, 1996). The first major advance in multi-subject analyses was the advent of objective normalization procedures for PET imaging (Fox et al., 1985). Fox et al. developed a stereotaxic transform for individual subjects to a common reference space, which was the first objective approach used to normalize subjects (Fox et al., 1985). Importantly, this method enabled the use of a common atlas space and improved power by allowing the analyses across subjects. Another critical advance was the development of imaging atlases in a standard coordinate space (e.g. MNI152) created from many individuals (Evans et al., 1993, Evans et al., 1994, Mazziotta et al., 2001, Mazziotta et al., 1995). The standardized atlas serves as a target space to which any individual brain can be spatially normalized, and provides a standard coordinate system to report results and thereby enhance comparisons and generalizability across labs. Such approaches are now the standard in human brain mapping methodologies including functional imaging with fMRI and PET using voxel-based (Ashburner et al., 1998, Woods et al., 1999, Woods et al., 1998a, Woods et al., 1998b, Zeffiro et al., 1997) and surface-based (Fischl et al., 1999, Van Essen, 2005) methods (though different standard atlas spaces exist—see Devlin and Poldrack, 2007).

Accessible population-average atlases in a standard coordinate space for non-human primate (NHP) species, such as rhesus macaque (Macaca mulatta), are less common. Although atlases exist for the rhesus macaque, they are based on post-mortem slices (Martin and Bowden, 1996, Mikula et al., 2007, Paxinos et al., 2000) and thus do not provide an accessible MRI target to which individual animals can be spatially normalized. Furthermore, atlases are typically based on a single subject and are thus less likely to be representative of the population.

There are currently a handful of NHP atlases available to the imaging community. Most of these atlases are based on a single animal (Cannestra et al., 1997, Saleem and Logothetis, 2006, Van Essen, 2002, Van Essen, 2004); while others are based on small samples of 6–12 animals (Black et al., 2001a, Black et al., 2001b, Greer et al., 2002, Vincent et al., 2007). NHP atlases that are based on multiple animals capture more of the variability in the species from which they were drawn, and for this reason may be preferable to single-subject atlases. However, due to inter-species variability, NHP atlases should be species-specific. Examples of species-specific non-human primate multi-subject, population-average atlases include Macaca nemestrina (Black et al., 2001a; see—http://www.nil.wustl.edu/labs/kevin/ni/n2k/ and http://www.loni.ucla.edu/Atlases/Atlas_Detail.jsp?atlas_id=2; 2004), Macaca fascicularis (Vincent et al., 2007; also see—http://www.nil.wustl.edu/labs/kevin/ni/cyno/cyno.html), Papio anubis (Black et al., 2001b; see—http://www.nil.wustl.edu/labs/kevin/ni/b2k/; Greer et al., 2002). Black et al. studied nine P. anubis to create the first probabilistic NHP atlas. Briefly, their method aligned their baboons to the Davis and Huffman atlas (Davis and Huffman, 1968), averaged them together to create an initial average, aligned the average to the atlas, and then aligned their baboons to the initial average, averaged the individuals again, and aligned the average to the Davis and Huffman atlas with 20 iterations (Black et al., 1997, Black et al., 2001b).

The rhesus macaque is a very commonly studied NHP species for which a population-average atlas does not exist; the development for such an atlas is the focus of this report. This atlas is based on the coordinate space of the single-subject atlas of Saleem-Logothetis (D99-SL) which includes MRI sections coregistered to histological slices (nissl, parvalbumin, SMI-32, calbindin and calretinin) and cytoarchitectonic areas (Saleem and Logothetis, 2006). We created a T1-weighted population-average template in the space of D99-SL. In addition, we present probabilistic tissue classification maps, prior probability maps, that can improve tissue segmentation in NHP MR images and illustrate their application. We also created T2-weighted atlas to complement the T1-weighted volume atlas. Finally, we created a transform to the F99 surface-based atlas to facilitate comparisons with other primate species (e.g. humans and fascicularis macaques, see—Van Essen and Dierker, 2007).

Section snippets

Materials and methods

Eighty-two male and thirty female rhesus macaques (M. mulatta) underwent MR imaging at one of three imaging sites. Rhesus macaque demographics are detailed in Table 1. All monkeys belonged to existing primate colonies at one of three sites: the National Institutes of Health Animal Center (NIHAC) in Poolesville, MD, USA; the Oregon National Primate Research Center at the Oregon Health and Science University (ONPRC/OHSU) in Beaverton, OR, USA; the Wisconsin National Primate Research Center at the

Atlases

Using the processing stream outlined in Fig. 1, we formed a T1-weighted atlas, 112RM-SL, (Fig. 2 middle, http://sumsdb.wustl.edu/sums/directory.do?id=6716882&dir_name=MCLAREN_EtAl_2009 and http://www.brainmap.wisc.edu/monkey.html), which is in register with the single-subject D99-SL atlas (Fig. 2 top) and thus are explicitly associated with published histology (Saleem and Logothetis, 2006). Fig. 2 (bottom) illustrates the T2-weighted atlas, which is also in register with the single subject

Species-specific atlases

The dramatic variation in global brain volume within the Macaca genus (fascicularis [left hemisphere — 29.37 cm3] < mulatta [80 cm3] < nemestrina [97.7 cm3]) suggests the need to have separate atlases for different species (Dorph-Petersen et al., 2005, Franklin et al., 2000, Malkova et al., 2006). Bowden and Dubach suggest that the size differences may be correctable by global scaling; however, they acknowledge that their analysis was limited to the brainstem region and not the entire cortex (

Conclusion

Brain imaging in non-human primates is becoming increasingly common for many experimental applications. Here we present a brain atlas collection for the adult rhesus macaque (M. mulatta) and review methods for creating multi-modal atlases using an infrastructure that will allow voxel- and surface-based approaches that are common in human brain mapping studies to be readily applied to non-human primate studies. More importantly, these atlases provide a standardized space that will allow

Acknowledgments

This study was supported in part by the National Institutes of Health RR000167 (UW), AG11915 (UW), AG20013 (UW), GM007507 (UW), RR00163 (ONPRC), AG029612 (OHSU) and the Intramural Research Program of the National Institute on Aging. This study was also supported with resources and use of facilities at the William S. Middleton Memorial Veterans Hospital, Madison, WI, USA. John Matochik is now at the National Institute on Alcohol Abuse and Alcoholism. The assistance of Erik K. Kastman, Brent W.

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