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Article: Automatic Geometry-based Estimation of the Locus Coeruleus Region on T

Aganj, Iman / Mora, Jocelyn / Fischl, Bruce / Augustinack, Jean C

bioRxiv : the preprint server for biology

2024

Abstract: The locus coeruleus (LC) is a key brain structure implicated in cognitive function and neurodegenerative disease. Automatic segmentation of the LC is a crucial step in quantitative non-invasive analysis of the LC in large MRI cohorts. Most publicly ... ...

Abstract	The locus coeruleus (LC) is a key brain structure implicated in cognitive function and neurodegenerative disease. Automatic segmentation of the LC is a crucial step in quantitative non-invasive analysis of the LC in large MRI cohorts. Most publicly available imaging databases for training automatic LC segmentation models take advantage of specialized contrast-enhancing (e.g., neuromelanin-sensitive) MRI. Segmentation models developed with such image contrasts, however, are not readily applicable to existing datasets with conventional MRI sequences. In this work, we evaluate the feasibility of using non-contrast neuroanatomical information to geometrically approximate the LC region from standard 3-Tesla T
Language	English
Publishing date	2024-01-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.23.576958
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Article ; Online: The prosubiculum in the human hippocampus: A rostrocaudal, feature-driven, and systematic approach.

Rosenblum, Emma W / Williams, Emily M / Champion, Samantha N / Frosch, Matthew P / Augustinack, Jean C

The Journal of comparative neurology

2024 Volume 532, Issue 3, Page(s) e25604

Abstract: The hippocampal subfield prosubiculum (ProS), is a conserved neuroanatomic region in mouse, monkey, and human. This area lies between CA1 and subiculum (Sub) and particularly lacks consensus on its boundaries; reports have varied on the description of ... ...

Abstract	The hippocampal subfield prosubiculum (ProS), is a conserved neuroanatomic region in mouse, monkey, and human. This area lies between CA1 and subiculum (Sub) and particularly lacks consensus on its boundaries; reports have varied on the description of its features and location. In this report, we review, refine, and evaluate four cytoarchitectural features that differentiate ProS from its neighboring subfields: (1) small neurons, (2) lightly stained neurons, (3) superficial clustered neurons, and (4) a cell sparse zone. ProS was delineated in all cases (n = 10). ProS was examined for its cytoarchitectonic features and location rostrocaudally, from the anterior head through the body in the hippocampus. The most common feature was small pyramidal neurons, which were intermingled with larger pyramidal neurons in ProS. We quantitatively measured ProS pyramidal neurons, which showed (average, width at pyramidal base = 14.31 µm, n = 400 per subfield). CA1 neurons averaged 15.57 µm and Sub neurons averaged 15.63 µm, both were significantly different than ProS (Kruskal-Wallis test, p < .0001). The other three features observed were lightly stained neurons, clustered neurons, and a cell sparse zone. Taken together, these findings suggest that ProS is an independent subfield, likely with distinct functional contributions to the broader interconnected hippocampal network. Our results suggest that ProS is a cytoarchitecturally varied subfield, both for features and among individuals. This diverse architecture in features and individuals for ProS could explain the long-standing complexity regarding the identification of this subfield.
MeSH term(s)	Humans ; Mice ; Animals ; Hippocampus/physiology ; Neurons ; Pyramidal Cells/physiology
Language	English
Publishing date	2024-03-13
Publishing country	United States
Document type	Review ; Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.25604
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Article: Quantitative optical coherence microscopy of neuron morphology in human entorhinal cortex.

Wang, Hui / Gong, Dayang / Augustinack, Jean C / Magnain, Caroline

Frontiers in neuroscience

2023 Volume 17, Page(s) 1074660

Abstract: Introduction: The size and shape of neurons are important features indicating aging and the pathology of neurodegenerative diseases. Despite the significant advances of optical microscopy, quantitative analysis of the neuronal features in the human ... ...

Abstract	Introduction: The size and shape of neurons are important features indicating aging and the pathology of neurodegenerative diseases. Despite the significant advances of optical microscopy, quantitative analysis of the neuronal features in the human brain remains largely incomplete. Traditional histology on thin slices bears tremendous distortions in three-dimensional reconstruction, the magnitude of which are often greater than the structure of interest. Recently development of tissue clearing techniques enable the whole brain to be analyzed in small animals; however, the application in the human remains challenging. Methods: In this study, we present a label-free quantitative optical coherence microscopy (OCM) technique to obtain the morphological parameters of neurons in human entorhinal cortex (EC). OCM uses the intrinsic back-scattering property of tissue to identify individual neurons in 3D. The area, length, width, and orientation of individual neurons are quantified and compared between layer II and III in EC. Results: The high-resolution mapping of neuron size, shape, and orientation shows significant differences between layer II and III neurons in EC. The results are validated by standard Nissl staining of the same samples. Discussion: The quantitative OCM technique in our study offers a new solution to analyze variety of neurons and their organizations in the human brain, which opens new insights in advancing our understanding of neurodegenerative diseases.
Language	English
Publishing date	2023-04-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2411902-7
ISSN	1662-453X ; 1662-4548
ISSN (online)	1662-453X
ISSN	1662-4548
DOI	10.3389/fnins.2023.1074660
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Article ; Online: TDP-43 and tau concurrence in the entorhinal subfields in primary age-related tauopathy and preclinical Alzheimer's disease.

Llamas-Rodríguez, Josué / Oltmer, Jan / Marshall, Michael / Champion, Samantha / Frosch, Matthew P / Augustinack, Jean C

Brain pathology (Zurich, Switzerland)

2023 Volume 33, Issue 4, Page(s) e13159

Abstract: Phosphorylated tau (p-tau) pathology correlates strongly with cognitive decline and is a pathological hallmark of Alzheimer's Disease (AD). In recent years, phosphorylated transactive response DNA-binding protein (pTDP-43) has emerged as a common ... ...

Abstract	Phosphorylated tau (p-tau) pathology correlates strongly with cognitive decline and is a pathological hallmark of Alzheimer's Disease (AD). In recent years, phosphorylated transactive response DNA-binding protein (pTDP-43) has emerged as a common comorbidity, found in up to 70% of all AD cases (Josephs et al., Acta Neuropathol, 131(4), 571-585; Josephs, Whitwell, et al., Acta Neuropathol, 127(6), 811-824). Current staging schemes for pTDP-43 in AD and primary age-related tauopathy (PART) track its progression throughout the brain, but the distribution of pTDP-43 within the entorhinal cortex (EC) at the earliest stages has not been studied. Moreover, the exact nature of p-tau and pTDP-43 co-localization is debated. We investigated the selective vulnerability of the entorhinal subfields to phosphorylated pTDP-43 pathology in preclinical AD and PART postmortem tissue. Within the EC, posterior-lateral subfields showed the highest semi-quantitative pTDP-43 density scores, while the anterior-medial subfields had the lowest. On the rostrocaudal axis, pTDP-43 scores were higher posteriorly than anteriorly (p < 0.010), peaking at the posterior-most level (p < 0.050). Further, we showed the relationship between pTDP-43 and p-tau in these regions at pathology-positive but clinically silent stages. P-tau and pTDP-43 presented a similar pattern of affected subregions (p < 0.0001) but differed in density magnitude (p < 0.0001). P-tau burden was consistently higher than pTDP-43 at every anterior-posterior level and in most EC subfields. These findings highlight pTDP-43 burden heterogeneity within the EC and the posterior-lateral subfields as the most vulnerable regions within stage II of the current pTDP-43 staging schemes for AD and PART. The EC is a point of convergence for p-tau and pTDP-43 and identifying its most vulnerable neuronal populations will prove key for early diagnosis and disease intervention.
MeSH term(s)	Humans ; Alzheimer Disease/pathology ; Tauopathies/pathology ; tau Proteins/metabolism ; DNA-Binding Proteins/metabolism ; Entorhinal Cortex/metabolism ; Brain/pathology
Chemical Substances	tau Proteins ; DNA-Binding Proteins
Language	English
Publishing date	2023-04-10
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1051484-3
ISSN	1750-3639 ; 1015-6305
ISSN (online)	1750-3639
ISSN	1015-6305
DOI	10.1111/bpa.13159
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Article: Pentad: A reproducible cytoarchitectonic protocol and its application to parcellation of the human hippocampus.

Williams, Emily M / Rosenblum, Emma W / Pihlstrom, Nicole / Llamas-Rodríguez, Josué / Champion, Samantha / Frosch, Matthew P / Augustinack, Jean C

Frontiers in neuroanatomy

2023 Volume 17, Page(s) 1114757

Abstract: Introduction: The hippocampus is integral for learning and memory and is targeted by multiple diseases. Neuroimaging approaches frequently use hippocampal subfield volumes as a standard measure of neurodegeneration, thus making them an essential ... ...

Abstract	Introduction: The hippocampus is integral for learning and memory and is targeted by multiple diseases. Neuroimaging approaches frequently use hippocampal subfield volumes as a standard measure of neurodegeneration, thus making them an essential biomarker to study. Collectively, histologic parcellation studies contain various disagreements, discrepancies, and omissions. The present study aimed to advance the hippocampal subfield segmentation field by establishing the first histology based parcellation protocol, applied to Methods: The protocol focuses on five cellular traits observed in the pyramidal layer of the human hippocampus. We coin this approach the pentad protocol. The traits were: chromophilia, neuron size, packing density, clustering, and collinearity. Subfields included were CA1, CA2, CA3, CA4, prosubiculum, subiculum, presubiculum, parasubiculum, as well as the medial (uncal) subfields Subu, CA1u, CA2u, CA3u, and CA4u. We also establish nine distinct anterior-posterior levels of the hippocampus in the coronal plane to document rostrocaudal differences. Results: Applying the pentad protocol, we parcellated 13 subfields at nine levels in 22 samples. We found that CA1 had the smallest neurons, CA2 showed high neuronal clustering, and CA3 displayed the most collinear neurons of the CA fields. The border between presubiculum and subiculum was staircase shaped, and parasubiculum had larger neurons than presubiculum. We also demonstrate cytoarchitectural evidence that CA4 and prosubiculum exist as individual subfields. Discussion: This protocol is comprehensive, regimented and supplies a high number of samples, hippocampal subfields, and anterior-posterior coronal levels. The pentad protocol utilizes the gold standard approach for the human hippocampus subfield parcellation.
Language	English
Publishing date	2023-02-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452969-2
ISSN	1662-5129
ISSN	1662-5129
DOI	10.3389/fnana.2023.1114757
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Article: Quantitative imaging of three-dimensional fiber orientation in the human brain via two illumination angles using polarization-sensitive optical coherence tomography.

Liu, Chao J / Ammon, William / Jones, Robert J / Nolan, Jackson C / Gong, Dayang / Maffei, Chiara / Edlow, Brian L / Augustinack, Jean C / Magnain, Caroline / Yendiki, Anastasia / Villiger, Martin / Fischl, Bruce / Wang, Hui

bioRxiv : the preprint server for biology

2023

Abstract: The accurate measurement of three-dimensional (3D) fiber orientation in the brain is crucial for reconstructing fiber pathways and studying their involvement in neurological diseases. Optical imaging methods such as polarization-sensitive optical ... ...

Abstract	The accurate measurement of three-dimensional (3D) fiber orientation in the brain is crucial for reconstructing fiber pathways and studying their involvement in neurological diseases. Optical imaging methods such as polarization-sensitive optical coherence tomography (PS-OCT) provide important tools to directly quantify fiber orientation at micrometer resolution. However, brain imaging based on the optic axis by PS-OCT so far has been limited to two-dimensional in-plane orientation, preventing the comprehensive study of connectivity in 3D. In this work, we present a novel method to obtain the 3D fiber orientation in full angular space with only two illumination angles. We measure the optic axis orientation and the apparent birefringence by PS-OCT from a normal and a 15 deg tilted illumination, and then apply a computational method yielding the 3D optic axis orientation and true birefringence. We verify that our method accurately recovers a large range of through-plane orientations from -85 deg to 85 deg with a high angular precision. We further present 3D fiber orientation maps of entire coronal sections of human cerebrum and brainstem with 10 μm in-plane resolution, revealing unprecedented details of fiber configurations. We envision that further development of our method will open a promising avenue towards large-scale 3D fiber axis mapping in the human brain and other complex fibrous tissues at microscopic level.
Language	English
Publishing date	2023-10-23
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.20.563298
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Article: Multi-Scale Label-free Human Brain Imaging with Integrated Serial Sectioning Polarization Sensitive Optical Coherence Tomography and Two-Photon Microscopy.

Chang, Shuaibin / Yang, Jiarui / Novoseltseva, Anna / Fu, Xinlei / Li, Chenglin / Chen, Shih-Chi / Augustinack, Jean C / Magnain, Caroline / Fischl, Bruce / Mckee, Ann C / Boas, David A / Chen, Ichun Anderson / Wang, Hui

bioRxiv : the preprint server for biology

2023

Abstract: The study of neurodegenerative processes in the human brain requires a comprehensive understanding of cytoarchitectonic, myeloarchitectonic, and vascular structures. Recent computational advances have enabled volumetric reconstruction of the human brain ... ...

Abstract	The study of neurodegenerative processes in the human brain requires a comprehensive understanding of cytoarchitectonic, myeloarchitectonic, and vascular structures. Recent computational advances have enabled volumetric reconstruction of the human brain using thousands of stained slices, however, tissue distortions and loss resulting from standard histological processing have hindered deformation-free reconstruction of the human brain. The development of a multi-scale and volumetric human brain imaging technique that can measure intact brain structure would be a major technical advance. Here, we describe the development of integrated serial sectioning Polarization Sensitive Optical Coherence Tomography (PSOCT) and Two Photon Microscopy (2PM) to provide label-free multi-contrast imaging, including scattering, birefringence and autofluorescence of human brain tissue. We demonstrate that high-throughput reconstruction of 4×4×2cm
Language	English
Publishing date	2023-05-24
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.22.541785
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Article ; Online: Stereology neuron counts correlate with deep learning estimates in the human hippocampal subregions.

Oltmer, Jan / Rosenblum, Emma W / Williams, Emily M / Roy, Jessica / Llamas-Rodriguez, Josué / Perosa, Valentina / Champion, Samantha N / Frosch, Matthew P / Augustinack, Jean C

Scientific reports

2023 Volume 13, Issue 1, Page(s) 5884

Abstract: Hippocampal subregions differ in specialization and vulnerability to cell death. Neuron death and hippocampal atrophy have been a marker for the progression of Alzheimer's disease. Relatively few studies have examined neuronal loss in the human brain ... ...

Abstract	Hippocampal subregions differ in specialization and vulnerability to cell death. Neuron death and hippocampal atrophy have been a marker for the progression of Alzheimer's disease. Relatively few studies have examined neuronal loss in the human brain using stereology. We characterize an automated high-throughput deep learning pipeline to segment hippocampal pyramidal neurons, generate pyramidal neuron estimates within the human hippocampal subfields, and relate our results to stereology neuron counts. Based on seven cases and 168 partitions, we vet deep learning parameters to segment hippocampal pyramidal neurons from the background using the open-source CellPose algorithm, and show the automated removal of false-positive segmentations. There was no difference in Dice scores between neurons segmented by the deep learning pipeline and manual segmentations (Independent Samples t-Test: t(28) = 0.33, p = 0.742). Deep-learning neuron estimates strongly correlate with manual stereological counts per subregion (Spearman's correlation (n = 9): r(7) = 0.97, p < 0.001), and for each partition individually (Spearman's correlation (n = 168): r(166) = 0.90, p <0 .001). The high-throughput deep-learning pipeline provides validation to existing standards. This deep learning approach may benefit future studies in tracking baseline and resilient healthy aging to the earliest disease progression.
MeSH term(s)	Humans ; Deep Learning ; Image Processing, Computer-Assisted/methods ; Hippocampus ; Neurons ; Brain
Language	English
Publishing date	2023-04-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-32903-y
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Article ; Online: Assessing individual variability of the entorhinal subfields in health and disease.

Oltmer, Jan / Greve, Douglas N / Cerri, Stefano / Slepneva, Natalya / Llamas-Rodríguez, Josue / Iglesias, Juan Eugenio / Van Leemput, Koen / Champion, Samantha N / Frosch, Matthew P / Augustinack, Jean C

The Journal of comparative neurology

2023 Volume 531, Issue 18, Page(s) 2062–2079

Abstract: Investigating interindividual variability is a major field of interest in neuroscience. The entorhinal cortex (EC) is essential for memory and affected early in the progression of Alzheimer's disease (AD). We combined histology ground-truth data with ... ...

Abstract	Investigating interindividual variability is a major field of interest in neuroscience. The entorhinal cortex (EC) is essential for memory and affected early in the progression of Alzheimer's disease (AD). We combined histology ground-truth data with ultrahigh-resolution 7T ex vivo MRI to analyze EC interindividual variability in 3D. Further, we characterized (1) entorhinal shape as a whole, (2) entorhinal subfield range and midpoints, and (3) subfield architectural location and tau burden derived from 3D probability maps. Our results indicated that EC shape varied but was not related to demographic or disease factors at this preclinical stage. The medial intermediate subfield showed the highest degree of location variability in the probability maps. However, individual subfields did not display the same level of variability across dimensions and outcome measure, each providing a different perspective. For example, the olfactory subfield showed low variability in midpoint location in the superior-inferior dimension but high variability in anterior-posterior, and the subfield entorhinal intermediate showed a large variability in volumetric measures but a low variability in location derived from the 3D probability maps. These findings suggest that interindividual variability within the entorhinal subfields requires a 3D approach incorporating multiple outcome measures. This study provides 3D probability maps of the individual entorhinal subfields and respective tau pathology in the preclinical stage (Braak I and II) of AD. These probability maps illustrate the subfield average and may serve as a checkpoint for future modeling.
MeSH term(s)	Humans ; Hippocampus/pathology ; Magnetic Resonance Imaging/methods ; Entorhinal Cortex ; Alzheimer Disease/diagnostic imaging ; Alzheimer Disease/pathology
Language	English
Publishing date	2023-09-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.25538
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Article: Harnessing advances in structural MRI to enhance research on Parkinson's disease.

Ziegler, David A / Augustinack, Jean C

Imaging in medicine

2013 Volume 5, Issue 2, Page(s) 91–94

Language	English
Publishing date	2013-04-27
Publishing country	England
Document type	Journal Article
ZDB-ID	2537201-4
ISSN	1755-5205 ; 1755-5191
ISSN (online)	1755-5205
ISSN	1755-5191
DOI	10.2217/iim.13.8
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