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Basal Forebrain Published June 13, 2019 as 10.3174/ajnr.A6088 ORIGINAL RESEARCH ADULT BRAIN 3T MRI Whole-Brain Microscopy Discrimination of Subcortical Anatomy, Part 2: Basal Forebrain X M.J. Hoch, X M.T. Bruno, X A. Faustin, X N. Cruz, X A.Y. Mogilner, X L. Crandall, X T. Wisniewski, X O. Devinsky, and X T.M. Shepherd ABSTRACT BACKGROUND AND PURPOSE: The basal forebrain contains multiple structures of great interest to emerging functional neurosurgery applications, yet many neuroradiologists are unfamiliar with this neuroanatomy because it is not resolved with current clinical MR imaging. MATERIALS AND METHODS: We applied an optimized TSE T2 sequence to washed whole postmortem brain samples (n ϭ 13) to demonstrate and characterize the detailed anatomy of the basal forebrain using a clinical 3T MR imaging scanner. We measured the size of selected internal myelinated pathways and measured subthalamic nucleus size, oblique orientation, and position relative to the intercommissural point. RESULTS: We identified most basal ganglia and diencephalon structures using serial axial, coronal, and sagittal planes relative to the intercommissural plane. Specific oblique image orientations demonstrated the positions and anatomic relationships for selected struc- tures of interest to functional neurosurgery. We observed only 0.2- to 0.3-mm right-left differences in the anteroposterior and supero- inferior length of the subthalamic nucleus (P ϭ .084 and .047, respectively). Individual variability for the subthalamic nucleus was greatest for angulation within thesagittal plane (range, 15°–37°), transverse dimension (range, 2–6.7 mm), and most inferior border (range, 4–7 mm below the intercommissural plane). CONCLUSIONS: Direct identification of basal forebrain structures in multiple planes using the TSE T2 sequence makes this challenging neuroanatomy more accessible to practicing neuroradiologists. This protocol can be used to better define individual variations relevant to functional neurosurgical targeting and validate/complement advanced MR imaging methods being developed for direct visualization of these structures in living patients. ABBREVIATIONS: DBS ϭ deep brain stimulation; DRT ϭ dentatorubrothalamic tract; PLIC ϭ posterior limb of the internal capsule; STN ϭ subthalamic nucleus; SUDC ϭ sudden unexplained death of childhood; Vim ϭ thalamic ventrointermedius nucleus; ZI ϭ zona incerta eep to the cortical surface, the basal ganglia, thalamus, and exceeds the cerebral cortex in the resting state.3 Focal pathologic Dsubthalamus are vital basal forebrain structures involved in functional or structural changes can have serious clinical conse- the regulation of autonomic, motor, sensory, limbic, and endo- quences due to the compact organization of the basal forebrain. crine functions.1,2 The metabolic demand of the basal forebrain The thalamus is a complex hub receiving subcortical sensory and motor input that projects to both the cortex and striatum.4 Tha- lamic infarction, demyelination, tumors, and other pathologies Received March 9, 2019; accepted after revision April 22. can cause chronic pain,5 sensory loss in multiple modalities, am- From the Department of Radiology and Imaging Sciences, (M.J.H.), Emory Univer- nesia,6 dystonia,7 and other disorders.8,9 The subthalamus mod- sity, Atlanta, Georgia; Departments of Radiology (M.T.B., N.C., T.M.S.), Pathology 10 (A.F., T.W.), Neurosurgery (A.Y.M.), Neurology (L.C., T.W., O.D.), and Psychiatry ulates basal ganglia output. Ischemic and hyperglycemic inju- (T.W.), New York University, New York, New York; SUDC Foundation (L.C., O.D.), ries of the subthalamic nucleus can result in hemiballism.11,12 The New York, New York; and Center for Advanced Imaging Innovation and Research (T.M.S.), New York, New York. basal ganglia have complex connections to the cortical motor This study was funded by the SUDC Foundation, the Taylor McKeen Shelton Foun- areas, including the precentral gyrus, supplementary motor dation, and the Finding a Cure for Epilepsy and Seizures fund. T.M.S. received re- 13 search support from the National Institute of Aging (grant AG048622). T.W. and area, and frontal eye fields. Basal ganglia pathologies cause A.F. received research support from the National Institute of Aging (grant AG008051). This work was supported, in part, by the Center for Advanced Imaging Indicates open access to non-subscribers at www.ajnr.org Innovation and Research, a National Institutes of Health–National Institute of Bio- medical Imaging and Bioengineering Biomedical Technology Resource Center article with supplemental on-line photos. (Grant P41EB017183). Indicates article with supplemental on-line videos. Please address correspondence to Timothy Shepherd, 660 First Ave, Room 226, New York, NY, 10016; e-mail: [email protected] http://dx.doi.org/10.3174/ajnr.A6088 AJNR Am J Neuroradiol ●:●●2019 www.ajnr.org 1 Copyright 2019 by American Society of Neuroradiology. movement disorders (eg, Parkinson, Huntington, and Wilson aging relaxation changes from the free aldehyde fixative solu- diseases), developmental disorders (eg, autism), or neuropsy- tion.40 Individual brains with MR imaging data included for the chiatric disorders (eg, Tourette syndrome and obsessive-com- figures (n ϭ 13) in this study met the following criteria: 1) mini- pulsive disorder).14-17 mal injury to cerebral hemispheres or callosum from procure- Functional neurosurgery is a rapidly evolving field with mul- ment, 2) no MR imaging or pathologic abnormality (outside the tiple basal forebrain targets to reversibly inhibit selected struc- hippocampus) identified by a board-certified neuroradiologist tures with deep brain stimulation (DBS) or ablate those structures and neuropathologist, respectively, 3) no T1-hyperintense fixa- using MR imaging–guided focused sonography. The subthalamic tion bands in the basal forebrain structures due to variable fixa- nucleus (STN), globus pallidus internus, and thalamic ventroin- tion penetration,41 and 4) a prerefrigeration postmortem interval termedius nucleus (Vim) are common targets to treat medically of Ͻ24 hours.42 One of 14 consecutive SUDC samples was re- refractory hypo- and hyperkinetic movement disorders.18 Ex- jected due to procurement-induced division of the midbrain. The ploratory targets include the habenulopeduncular pathway or nu- mean postnatal age for included specimens was 47.3 Ϯ 34.8 cleus accumbens for treating refractory depression and substance months with a range between 22 and 142 months (10/13 speci- abuse.19,20 Chronic electrical stimulation of selected thalamic mens were between 24 and 48 months of age); 6/13 specimens subnuclei can reduce seizures in patients with epilepsy.21 Despite were from male subjects with SUDC. After imaging was com- therapeutic successes, the mechanisms of DBS remain incom- pleted, brains were returned to the SUDC research study for brain pletely explained, partially due to limited anatomic and func- cutting within 7–10 days. tional understanding of key structures. For example, DBS of the STN is used to treat Parkinson disease, though some suggest zona Whole-Brain MR Imaging Protocol incerta stimulation may also be clinically important.22,23 Each brain was immersed in water inside a custom 3D-printed Imaging tools to precisely define basal forebrain structures container specifically designed to conform to a 64-channel head remain relatively unchanged despite rapid advances in therapeu- and neck coil on a 3T Prisma MR imaging scanner (Siemens, tics. To better understand the best anatomic targets and the actual Erlangen, Germany). Sealed water-filled disposable powderless mechanism for clinical improvement observed with functional latex medical gloves were gently wedged between the container neurosurgery, we need to directly visualize the relevant functional and brain to prevent motion. Scout sequences identified the brain anatomy before and ideally after treatment. Conventional MR position, and then 2D, high-resolution TSE MR imaging se- imaging has limited contrast resolution for basal forebrain anat- quences of the whole brain were obtained in coronal, sagittal, and omy; this is an active goal of MR imaging research. Susceptibility- axial planes relative to the intercommissural plane. Optimization weighted MR imaging,24-26 ultra-high-field in vivo MR imag- of sequence parameters for contrast resolution of small structures ing,27-29 and advanced diffusion techniques30-32 can improve in the postmortem brain using TSE sequences with 3T MR imag- localization of key basal forebrain structures but are challenging ing was reported separately.34 T2-weighted TSE sequence param- to implement into routine clinical practice. Independent valida- eters were the following: TR ϭ 5380 ms, TE ϭ 53 ms, echo-train tion of diffusion methods has been limited.33 We developed a length ϭ 7, echo spacing ϭ 10.8 ms, bandwidth ϭ 415 Hz/pixel, rapid 3T postmortem anatomic MR imaging protocol34 using an slice thickness and number ϭ 0.8 mm ϫ 116 (no interslice gap), optimized 2D-TSE sequence with a clinical 3T MR imaging system in-plane resolution ϭ 0.35 ϫ 0.35 mm, concatenations ϭ 2, av- and head coil available at most institutions. This protocol produces erages ϭ 10, total time ϭ 2 hours (full protocol available on re- exquisite anatomic contrast for subcortical structures comparable to quest). The current scanner software limits the number of slices to neuroanatomic atlases with histologic stains.2,35-37 Here, we demon- 128, so whole-brain imaging with isotropic 350-␮m voxels
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