A Semi-Automated Pipeline for the Segmentation of Rhesus Macaque Hippocampus: Validation across a Wide Age Range

This report outlines a neuroimaging pipeline that allows a robust, high-throughput, semi-automated, template-based protocol for segmenting the hippocampus in rhesus macaque (Macaca mulatta) monkeys ranging from 1 week to 260 weeks of age. The semiautomated component of this approach minimizes user effort while concurrently maximizing the benefit of human expertise by requiring as few as 10 landmarks to be placed on images of each hippocampus to guide registration. Any systematic errors in the normalization process are corrected using a machine-learning algorithm that has been trained by comparing manual and automated segmentations to identify systematic errors. These methods result in high spatial overlap and reliability when compared with the results of manual tracing protocols. They also dramatically reduce the time to acquire data, an important consideration in large-scale neuroradiological studies involving hundreds of MRI scans. Importantly, other than the initial generation of the unbiased template, this approach requires only modest neuroanatomical training. It has been validated for high-throughput studies of rhesus macaque hippocampal anatomy across a broad age range.

[1]  S. Joshi,et al.  Shape analysis of hippocampal surface structure in patients with unilateral mesial temporal sclerosis , 2000, Journal of Digital Imaging.

[2]  Martin Styner,et al.  Asymmetric bias in user guided segmentations of brain structures , 2012, NeuroImage.

[3]  D. Amaral,et al.  Hippocampal volume is preserved and fails to predict recognition memory impairment in aged rhesus monkeys (Macaca mulatta) , 2006, Neurobiology of Aging.

[4]  Brian B. Avants,et al.  The optimal template effect in hippocampus studies of diseased populations , 2010, NeuroImage.

[5]  S. Eliez,et al.  Hippocampal volume reduction in chromosome 22q11.2 deletion syndrome (22q11.2DS): A longitudinal study of morphometry and symptomatology , 2012, Psychiatry Research: Neuroimaging.

[6]  Rebecca C. Knickmeyer,et al.  Maturational trajectories of cortical brain development through the pubertal transition: unique species and sex differences in the monkey revealed through structural magnetic resonance imaging. , 2010, Cerebral cortex.

[7]  Dominique Hasboun,et al.  Anatomically constrained region deformation for the automated segmentation of the hippocampus and the amygdala: Method and validation on controls and patients with Alzheimer’s disease , 2007, NeuroImage.

[8]  R. Saunders,et al.  Longitudinal magnetic resonance imaging study of rhesus monkey brain development , 2006, The European journal of neuroscience.

[9]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[10]  Brian B. Avants,et al.  Sparse Unbiased Analysis of Anatomical Variance in Longitudinal Imaging , 2010, MICCAI.

[11]  Jocelyne Bachevalier,et al.  Maturation of the hippocampal formation and amygdala in Macaca mulatta: A volumetric magnetic resonance imaging study , 2010, Hippocampus.

[12]  Alexander Hammers,et al.  Fully Automatic Segmentation of the Hippocampus and the Amygdala from MRI Using Hybrid Prior Knowledge , 2007, MICCAI.

[13]  Brian B. Avants,et al.  A learning-based wrapper method to correct systematic errors in automatic image segmentation: Consistently improved performance in hippocampus, cortex and brain segmentation , 2011, NeuroImage.

[14]  N. Schuff,et al.  Longitudinal volumetric MRI change and rate of cognitive decline , 2005, Neurology.

[15]  Katharina Buerger,et al.  Review Perspectives for Multimodal Neurochemical and Imaging Biomarkers in Alzheimer's Disease , 2022 .

[16]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[17]  R. Mark Henkelman,et al.  Neuroanatomical analysis of the BTBR mouse model of autism using magnetic resonance imaging and diffusion tensor imaging , 2013, NeuroImage.

[18]  James C Gee,et al.  Appearance and incomplete label matching for diffeomorphic template based hippocampus segmentation , 2009, Hippocampus.

[19]  Michael I. Miller,et al.  Magnetic resonance imaging deformation-based segmentation of the hippocampus in patients with mesial temporal sclerosis and temporal lobe epilepsy , 2000, Journal of Digital Imaging.

[20]  S. Resnick,et al.  Measuring Size and Shape of the Hippocampus in MR Images Using a Deformable Shape Model , 2002, NeuroImage.

[21]  D. Amaral,et al.  The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All Ages , 2004, The Journal of Neuroscience.

[22]  Martin Styner,et al.  A comparison of automated segmentation and manual tracing for quantifying hippocampal and amygdala volumes , 2009, NeuroImage.

[23]  S. Joshi,et al.  Mesial temporal sclerosis and temporal lobe epilepsy: MR imaging deformation-based segmentation of the hippocampus in five patients. , 2000, Radiology.

[24]  Joost Janssen,et al.  Hippocampal volume change in schizophrenia. , 2010, The Journal of clinical psychiatry.

[25]  Evan Fletcher,et al.  Spatially localized hippocampal shape analysis in late‐life cognitive decline , 2009, Hippocampus.

[26]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.