Large deformation diffeomorphic metric mapping registration of reconstructed 3D histological section images and in vivo MR images

Abstract

Our current understanding of neuroanatomical abnormalities in neuropsychiatric diseases is based largely on magnetic resonance imaging (MRI) and post mortem histological analyses of the brain. Further advances in elucidating altered brain structure in these human conditions might emerge from combining MRI and histological methods. We propose a multistage method for registering 3D volumes reconstructed from histological sections to corresponding in vivo MRI volumes from the same subjects: (1) manual segmentation of white matter (WM), gray matter (GM) and cerebrospinal fluid (CSF) compartments in histological sections, (2) alignment of consecutive histological sections using 2D rigid transformation to construct a 3D histological image volume from the aligned sections, (3) registration of reconstructed 3D histological volumes to the corresponding 3D MRI volumes using 3D affine transformation, (4) intensity normalization of images via histogram matching, and (5) registration of the volumes via intensity based large deformation diffeomorphic metric (LDDMM) image matching algorithm. Here we demonstrate the utility of our method in the transfer of cytoarchitectonic information from histological sections to identify regions of interest in MRI scans of nine adult macaque brains for morphometric analyses. LDDMM improved the accuracy of the registration via decreased distances between GM/CSF surfaces after LDDMM (0.39 ± 0.13 mm) compared to distances after affine registration (0.76 ± 0.41 mm). Similarly, WM/GM distances decreased to 0.28 ± 0.16 mm after LDDMM compared to 0.54 ± 0.39 mm after affine registration. The multistage registration method may find broad application for mapping histologically based information, for example, receptor distributions, gene expression, onto MRI volumes.

Blockface histology with optical coherence tomography: A comparison with Nissl staining

“…Histology validation has linked ground truth cellular pattern with probabilistic whole-brain maps (Amunts et al, 1999; Schleicher et al, 1999; Amunts and Zilles, 2001; Fischl et al, 2008, 2009; Augustinack et al, 2013). However, human histology is labor intensive and leads to irremediable deformations due to blocking, cutting, mounting and staining, which render registration across slices and to other modalities difficult (Ceritoglu et al, 2010; Reuter et al, 2010; Augustinack et al, 2010; Reuter et al, 2012). …”

Registration of in-vivo to ex-vivo MRI of surgically resected specimens: A pipeline for histology to in-vivo registration

“…Many previous studies in MRI and histology registration (see Table 3 2004; Meyer et al, 2006;Lebenberg et al, 2010;Schormann et al, 1995;Yelnik et al, 2007;Osechinskiy and Kruggel, 2011;Bardinet et al, 2002), and furthermore many previous studies included evaluation on only one dataset (Malandain et al, 2004;Choe et al, 2011;Meyer et al, 2006;Schormann et al, 1995;Kim et al, 2000;Yelnik et al, 2007;Osechinskiy and Kruggel, 2011;Bardinet et al, 2002;Lazebnik et al, 2003). Of the studies that did report accuracy on more than one dataset, TRE ranged from sub-millimeter (Ceritoglu et al, 2010;Jacobs et al, 1999;Yang et al, 2012) to 3-5 mm (Liu et al, 2012;Singh et al, 2008). Techniques that reported sub-millimeter TRE were applied on either whole brain sections of rodents or serially sectioned histology of primates, thus the smaller scale of anatomy and lack of variable resection boundaries can explain the lower TRE relative to our method.…”

“…In the past two decades, there have also been many studies specifically dealing with in-vivo brain MRI to post-mortem histology. The majority of these studies focused on primates (Dauguet et al, 2007;Malandain et al, 2004;Breen et al, 2005;Ceritoglu et al, 2010;Choe et al, 2011) or rodents (Jacobs et al, 1999;Humm et al, 2003;Meyer et al, 2006;Lebenberg et al, 2010;Yang et al, 2012;Liu et al, 2012). The few studies that registered human brain MRIto histology were performed on wholebrain (Schormann et al, 1995;Kim et al, 2000;Singh et al, 2008), or single hemisphere (Yelnik et al, 2007;Osechinskiy and Kruggel, 2011) post-mortem serially sectioned data (Amunts et al, 2013) created a 3D model of single subject's brain using post-mortem histological sections reconstructed at 20 m isotropic resolution and registered it to a T1 average atlas created from 24 subjects.…”

Cortico-Cortical, Cortico-Striatal, and Cortico-Thalamic White Matter Fiber Tracts Generated in the Macaque Brain via Dynamic Programming

“…Generated tracts were also consistent with those from the Schmahmann and Pandya (2006) atlas. It should be possible to reproduce the tractography for the right hemisphere, but the focus on the left has been motivated by an ongoing study of histology and MRI analyses in a macaque model of fetal exposure to radiation in which only the left hemisphere is available (Ceritoglu et al, 2010;Selemon et al, 2013). It is worth noting that the vast majority of published tracer studies have traditionally focused on one side.…”