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Evan Calabrese

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11 papers

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YNIMG Journal 2021 Journal Article

A high-resolution interactive atlas of the human brainstem using magnetic resonance imaging

Syed M. Adil
Evan Calabrese
Lefko T. Charalambous
James J. Cook
Shervin Rahimpour
Ahmet F. Atik
Gary P. Cofer
Beth A. Parente

Conventional atlases of the human brainstem are limited by the inflexible, sparsely-sampled, two-dimensional nature of histology, or the low spatial resolution of conventional magnetic resonance imaging (MRI). Postmortem high-resolution MRI circumvents the challenges associated with both modalities. A single human brainstem specimen extending from the rostral diencephalon through the caudal medulla was prepared for imaging after the brain was removed from a 65-year-old male within 24 h of death. The specimen was formalin-fixed for two weeks, then rehydrated and placed in a custom-made MRI compatible tube and immersed in liquid fluorocarbon. MRI was performed in a 7-Tesla scanner with 120 unique diffusion directions. Acquisition time for anatomic and diffusion images were 14 h and 208 h, respectively. Segmentation was performed manually. Deterministic fiber tractography was done using strategically chosen regions of interest and avoidance, with manual editing using expert knowledge of human neuroanatomy. Anatomic and diffusion images were rendered with isotropic resolutions of 50 μm and 200 μm, respectively. Ninety different structures were segmented and labeled, and 11 different fiber bundles were rendered with tractography. The complete atlas is available online for interactive use at https://www.civmvoxport.vm.duke.edu/voxbase/login.php?return_url=%2Fvoxbase%2F. This atlas presents multiple contrasting datasets and selected tract reconstruction with unprecedented resolution for MR imaging of the human brainstem. There are immediate applications in neuroanatomical education, with the potential to serve future applications for neuroanatomical research and enhanced neurosurgical planning through "safe" zones of entry into the human brainstem.

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YNIMG Journal 2019 Journal Article

Structural mapping with fiber tractography of the human cuneate fasciculus at microscopic resolution in cervical region

Ahmet Fatih Atik
Evan Calabrese
Robert Gramer
Syed M. Adil
Shervin Rahimpour
Promila Pagadala
G. Allan Johnson
Shivanand P. Lad

Human spinal white matter tract anatomy has been mapped using post mortem histological information with the help of molecular tracing studies in animal models. This study used 7 Tesla diffusion MR tractography on a human cadaver that was harvested 24 hours post mortem to evaluate cuneate fasciculus anatomy in cervical spinal cord. Based on this method, for the first time much more nuanced tractographic anatomy was used to investigate possible new routes for cuneate fasciculus in the posterior and lateral funiculus. Additionally, current molecular tracing studies were reviewed, and confirmatory data was presented along with our radiological results. Both studies confirm that upon entry to the spinal cord, upper cervical level tracts (C1-2-3) travel inside lateral funiculus and lower level tracts travel medially inside the posterior funiculus after entry at posterolateral sulcus which is different than traditional knowledge of having cuneate fasciculus tracts concentrated in the lateral part of posterior funiculus.

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YNICL Journal 2018 Journal Article

Postmortem diffusion MRI of the entire human spinal cord at microscopic resolution

Evan Calabrese
Syed M. Adil
Gary Cofer
Christian S. Perone
Julien Cohen-Adad
Shivanand P. Lad
G. Allan Johnson

The human spinal cord is a central nervous system structure that plays an important role in normal motor and sensory function, and can be affected by many debilitating neurologic diseases. Due to its clinical importance, the spinal cord is frequently the subject of imaging research. Common methods for visualizing spinal cord anatomy and pathology include histology and magnetic resonance imaging (MRI), both of which have unique benefits and drawbacks. Postmortem microscopic resolution MRI of fixed specimens, sometimes referred to as magnetic resonance microscopy (MRM), combines many of the benefits inherent to both techniques. However, the elongated shape of the human spinal cord, along with hardware and scan time limitations, have restricted previous microscopic resolution MRI studies (both in vivo and ex vivo) to small sections of the cord. Here we present the first MRM dataset of the entire postmortem human spinal cord. These data include 50 μm isotropic resolution anatomic image data and 100 μm isotropic resolution diffusion data, made possible by a 280 h long multi-segment acquisition and automated image segment composition. We demonstrate the use of these data for spinal cord lesion detection, automated volumetric gray matter segmentation, and quantitative spinal cord morphometry including estimates of cross sectional dimensions and gray matter fraction throughout the length of the cord.

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YNICL Journal 2018 Journal Article

Repeated mild blast exposure in young adult rats results in dynamic and persistent microstructural changes in the brain

Alexandra Badea
Alaa Kamnaksh
Robert J. Anderson
Evan Calabrese
Joseph B. Long
Denes V. Agoston

A history of mild traumatic brain injury (mTBI), particularly repeated mTBI (rmTBI), has been identified as a risk factor for late-onset neurodegenerative conditions. The mild and transient nature of early symptoms often impedes diagnosis in young adults who are disproportionately affected by mTBIs. A proportion of the affected population will incur long-term behavioral and cognitive consequences but the underlying pathomechanism is currently unknown. Diffusion tensor imaging (DTI) provides sensitive and quantitative assessment of TBI-induced structural changes, including white matter injury, and may be used to predict long-term outcome. We used DTI in an animal model of blast rmTBI (rmbTBI) to quantify blast-induced structural changes at 7 and 90 days post-injury, and their evolution between the two time points. Young adult male rats (~P65 at injury) were exposed to repeated mild blast overpressure, or anesthetized as shams, and their fixed brains were imaged using high-field (7 T) MRI. We found that whole brain volumes similarly increased in injured and sham rats from 7 to 90 days. However, we detected localized volume increases in blast-exposed animals 7 days post-injury, mainly ipsilateral to incident blast waves. Affected regions included gray matter of the frontal association, cingulate, and motor cortex, thalamus, substantia nigra, and raphe nuclei (median and dorsal), as well as white matter of the internal capsule and cerebral peduncle. Conversely, we measured volume reductions in these and other regions, including the hippocampus and cerebellum, at 90 days post-injury. DTI also detected both transient and persistent microstructural changes following injury, with some changes showing distinct ipsilateral versus contralateral side differences relative to blast impact. Early changes in fractional anisotropy (FA) were subtle, becoming more prominent at 90 days in the cerebral and inferior cerebellar peduncles, and cerebellar white matter. Widespread increases in radial diffusivity (RD) and axial diffusivity (primary eigenvalue or E1) at 7 days post-injury largely subsided by 90 days, although RD was more sensitive than E1 at detecting white matter changes. E1 effects in gray and white matter, which paralleled increases in apparent diffusion, were likely more indicative of dysregulated water homeostasis than pathologic structural changes. Importantly, we found evidence for a different developmental trajectory following rmbTBI, as indicated by significant injury x age interactions on volume. Our findings demonstrate that rmbTBI initiates dynamic pathobiological processes that may negatively alter the course of late-stage neurodevelopment and adversely affect long-term cognitive and behavioral outcomes.

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YNIMG Journal 2015 Journal Article

A diffusion tensor MRI atlas of the postmortem rhesus macaque brain

Evan Calabrese
Alexandra Badea
Christopher L. Coe
Gabriele R. Lubach
Yundi Shi
Martin A. Styner
G. Allan Johnson

The rhesus macaque (Macaca mulatta) is the most widely used nonhuman primate for modeling the structure and function of the brain. Brain atlases, and particularly those based on magnetic resonance imaging (MRI), have become important tools for understanding normal brain structure, and for identifying structural abnormalities resulting from disease states, exposures, and/or aging. Diffusion tensor imaging (DTI)-based MRI brain atlases are widely used in both human and macaque brain imaging studies because of the unique contrasts, quantitative diffusion metrics, and diffusion tractography that they can provide. Previous MRI and DTI atlases of the rhesus brain have been limited by low contrast and/or low spatial resolution imaging. Here we present a microscopic resolution MRI/DTI atlas of the rhesus brain based on 10 postmortem brain specimens. The atlas includes both structural MRI and DTI image data, a detailed three-dimensional segmentation of 241 anatomic structures, diffusion tractography, cortical thickness estimates, and maps of anatomic variability among atlas specimens. This atlas incorporates many useful features from previous work, including anatomic label nomenclature and ontology, data orientation, and stereotaxic reference frame, and further extends prior analyses with the inclusion of high-resolution multi-contrast image data.

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YNIMG Journal 2015 Journal Article

Addendum to “Waxholm Space atlas of the Sprague Dawley rat brain” [NeuroImage 97 (2014) 374-386]

Eszter A. Papp
Trygve B. Leergaard
Evan Calabrese
G. Allan Johnson
Jan G. Bjaalie

The main focus of our original article was to describe the anatomical delineations constituting the first version of the WHS Sprague Dawley atlas, apply the Waxholm Space coordinate system, and publish the associated MRI/DTI template and segmentation volume in their original format. To increase usability of the dataset, we have recently shared an updated version of the volumetric image material (v1. 01). The aims of this addendum are to inform about the improvements in the updated dataset, in particular related to navigation in the WHS coordinate system, and provide guidance for transforming coordinates acquired in the first version of the atlas.

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YNIMG Journal 2014 Journal Article

Waxholm Space atlas of the Sprague Dawley rat brain

Eszter A. Papp
Trygve B. Leergaard
Evan Calabrese
G. Allan Johnson
Jan G. Bjaalie

Three-dimensional digital brain atlases represent an important new generation of neuroinformatics tools for understanding complex brain anatomy, assigning location to experimental data, and planning of experiments. We have acquired a microscopic resolution isotropic MRI and DTI atlasing template for the Sprague Dawley rat brain with 39μm isotropic voxels for the MRI volume and 78μm isotropic voxels for the DTI. Building on this template, we have delineated 76 major anatomical structures in the brain. Delineation criteria are provided for each structure. We have applied a spatial reference system based on internal brain landmarks according to the Waxholm Space standard, previously developed for the mouse brain, and furthermore connected this spatial reference system to the widely used stereotaxic coordinate system by identifying cranial sutures and related stereotaxic landmarks in the template using contrast given by the active staining technique applied to the tissue. With the release of the present atlasing template and anatomical delineations, we provide a new tool for spatial orientationanalysis of neuroanatomical location, and planning and guidance of experimental procedures in the rat brain. The use of Waxholm Space and related infrastructures will connect the atlas to interoperable resources and services for multi-level data integration and analysis across reference spaces.

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YNIMG Journal 2013 Journal Article

A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability

Evan Calabrese
Alexandra Badea
Charles Watson
G. Allan Johnson

There has been growing interest in the role of postnatal brain development in the etiology of several neurologic diseases. The rat has long been recognized as a powerful model system for studying neuropathology and the safety of pharmacologic treatments. However, the complex spatiotemporal changes that occur during rat neurodevelopment remain to be elucidated. This work establishes the first magnetic resonance histology (MRH) atlas of the developing rat brain, with an emphasis on quantitation. The atlas comprises five specimens at each of nine time points, imaged with eight distinct MR contrasts and segmented into 26 developmentally defined brain regions. The atlas was used to establish a timeline of morphometric changes and variability throughout neurodevelopment and represents a quantitative database of rat neurodevelopment for characterizing rat models of human neurologic disease.

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YNIMG Journal 2013 Journal Article

An ontology-based segmentation scheme for tracking postnatal changes in the developing rodent brain with MRI

Evan Calabrese
G. Allan Johnson
Charles Watson

The postnatal period of neurodevelopment has been implicated in a number of brain disorders including autism and schizophrenia. Rodent models have proven to be invaluable in advancing our understanding of the human brain, and will almost certainly play a pivotal role in future studies on postnatal neurodevelopment. The growing field of magnetic resonance microscopy has the potential to revolutionize our understanding of neurodevelopment, if it can be successfully and appropriately assimilated into the vast body of existing neuroscience research. In this study, we demonstrate the utility of a developmental neuro-ontology designed specifically for tracking regional changes in MR biomarkers throughout postnatal neurodevelopment. Using this ontological classification as a segmentation guide, we track regional changes in brain volume in rats between postnatal day zero and postnatal day 80 and demonstrate differential growth rates in axial versus paraxial brain regions. Both the ontology and the associated label volumes are provided as a foundation for future MR-based studies of postnatal neurodevelopment in normal and disease states.

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YNIMG Journal 2013 Journal Article

Diffusion tensor magnetic resonance histology reveals microstructural changes in the developing rat brain

Evan Calabrese
G. Allan Johnson

The postnatal period is a remarkably dynamic phase of brain growth and development characterized by large-scale macrostructural changes, as well as dramatic microstructural changes, including myelination and cortical layering. This crucial period of neurodevelopment is uniquely susceptible to a wide variety of insults that may lead to neurologic disease. MRI is an important tool for studying both normal and abnormal neurodevelopmental changes, and quantitative imaging strategies like diffusion tensor imaging (DTI) allow visualization of many of the complex microstructural changes that occur during postnatal life. Diffusion tensor magnetic resonance histology (DT-MRH) provides particularly unique insight into cytoarchitectural changes in the developing brain. In this study, we used DT-MRH to track microstructural changes in the rat brain throughout normal postnatal neurodevelopment. We provide examples of diffusion tensor parameter changes in both white matter and gray matter structures, and correlate these changes with changes in cytoarchitecture. Finally, we provide a comprehensive database of image sets as a foundation for future studies using DT-MRH to characterize abnormal neurodevelopment in rodent models of neurodevelopmental disease.

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YNIMG Journal 2012 Journal Article

A multidimensional magnetic resonance histology atlas of the Wistar rat brain

G. Allan Johnson
Evan Calabrese
Alexandra Badea
George Paxinos
Charles Watson

We have produced a multidimensional atlas of the adult Wistar rat brain based on magnetic resonance histology (MRH). This MR atlas has been carefully aligned with the widely used Paxinos–Watson atlas based on optical sections to allow comparisons between histochemical and immuno-marker data, and the use of the Paxinos–Watson abbreviation set. Our MR atlas attempts to make a seamless connection with the advantageous features of the Paxinos–Watson atlas, and to extend the utility of the data through the unique capabilities of MR histology: a) ability to view the brain in the skull with limited distortion from shrinkage or sectioning; b) isotropic spatial resolution, which permits sectioning along any arbitrary axis without loss of detail; c) three-dimensional (3D) images preserving spatial relationships; and d) widely varied contrast dependent on the unique properties of water protons. 3D diffusion tensor images (DTI) at what we believe to be the highest resolution ever attained in the rat provide unique insight into white matter structures and connectivity. The 3D isotropic data allow registration of multiple data sets into a common reference space to provide average atlases not possible with conventional histology. The resulting multidimensional atlas that combines Paxinos–Watson with multidimensional MRH images from multiple specimens provides a new, comprehensive view of the neuroanatomy of the rat and offers a collaborative platform for future rat brain studies.

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