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Anatomy and Three-Dimensional Reconstructions of the Brain of The THEANATOMICALRECORD262:429–439(2001) AnatomyandThree-Dimensional ReconstructionsoftheBrainofthe WhiteWhale(Delphinapterusleucas) FromMagneticResonanceImages LORIMARINO,1*TIMOTHYL.MURPHY,2 AMYL.DEWEERD,2 JOHNA.MORRIS,3 ARCHIBALDJ.FOBBS,4 NATHALIEHUMBLOT,4 5 2,3 SAMH.RIDGWAY, ANDJOHNI.JOHNSON 1NeuroscienceandBehavioralBiologyProgram,PsychologyBuilding, EmoryUniversity,Atlanta,Georgia 2RadiologyDepartment,MichiganStateUniversity,EastLansing,Michigan 3NeuroscienceProgram,MichiganStateUniversity,EastLansing,Michigan 4NationalMuseumofHealthandMedicine,ArmedForcesInstituteofPathology, Washington,DC 5NavyMarineMammalProgram,SanDiego,California ABSTRACT Magneticresonanceimagingoffersameansofobservingtheinternal structureofthebrainwheretraditionalproceduresofembedding,section- ing,staining,mounting,andmicroscopicexaminationofthousandsofsec- tionsarenotpractical.Furthermore,internalstructurescanbeanalyzedin theirprecisequantitativespatialinterrelationships,whichisdifficultto accomplishafterthespatialdistortionsoftenaccompanyinghistological processing.Forthesereasons,magneticresonanceimagingmakesspeci- mensthatweretraditionallydifficulttoanalyze,moreaccessible.Inthe presentstudy,imagesofthebrainofawhitewhale(Beluga)Delphinapterus leucaswerescannedinthecoronalplaneat119antero-posteriorlevels. Fromthesescans,acomputer-generatedthree-dimensionalmodelwascon- structedusingtheprogramsVoxelViewandVoxelMath(VitalImages,Inc.). Thismodel,whereindetailsofinternalandexternalmorphologyarerep- resentedinthree-dimensionalspace,wasthenresectionedinorthogonal planestoproducecorrespondingseriesof“virtual”sectionsinthehorizontal andsagittalplanes.Sectionsinallthreeplanesdisplaythesizesand positionsofsuchstructuresasthecorpuscallosum,internalcapsule,cere- bralpeduncles,cerebralventricles,certainthalamicnucleargroups,cau- datenucleus,ventralstriatum,pontinenuclei,cerebellarcortexandwhite matter,andallcerebralcorticalsulciandgyri.AnatRec262:429–439, 2001. ©2001Wiley-Liss,Inc. Keywords:brain;neuroanatomy;cetacean;odontocete;white whale;Beluga;MRI Odontocetes(toothedwhales,dolphins,andporpoises) manyothermammalianbrains,odontocetebrainmor- haveundergoneanumberofevolutionarymodifications phologyisunusualinmanyrespects.Researchershave fromtheirterrestrialancestralstate.Amongthese changeswasamajorincreaseinrelativebrainsize.Sev- eralmodernodontocetespeciespossessencephalization levelssecondonlytomodernhumanswhenbrain-body *Correspondenceto:LoriMarino,PhD,PsychologyBuilding, allometryistakenintoaccount(RidgwayandBrownson, EmoryUniversity,Atlanta,GA30322. 1984;Marino,1998).Anarguablyequallydramatictrans- E-mail:[email protected] formationofodontocetesoccurredintheanatomicalstruc- Received8May2000;Accepted19November2000 tureandorganizationoftheirbrains.Comparedwith Publishedonline28February2001 ©2001WILEY-LISS,INC. 430 MARINO ET AL. Fig. 1. Ventral surface of a three-dimensional digital reconstruction of the whole brain and labeled schematic illustration of the same image. stated that “…the lobular formations in the dolphin brain and features (Tarpley and Ridgway, 1994; Glezer et al., are organized in a pattern fundamentally different from 1995a,b), and ontogenesis (Oelschlager and Buhl, 1985; that seen in the brains of primates or carnivores” (Mor- Buhl and Oelschlager, 1988; Oelschlager and Kemp, gane et al., 1980). Because of the fifty-five to sixty million 1998). year divergence between cetaceans and other mammals, Although there are a number of published descriptions odontocete brains represent a blend of early mammalian of cetacean neuroanatomy (see Morgane et al., 1986; Ridg- features along with unique derived characteristics (Ridg- way, 1990; for reviews of this literature) there are only a way, 1986, 1990; Glezer et al., 1988; Manger et al., 1998). handful of studies in which morphometric analyses were The differences between odontocete and other mammalian conducted in a systematic way permitting quantitative brains of similar size are present at the level of cortical comparative analysis with other mammals (Jacobs et al., cytoarchitecture and immunohistochemistry (Garey et al., 1984; Johnson et al., 1984; Schwerdtfeger et al., 1984; 1985; Garey and Leuba, 1986; Glezer and Morgane, 1990; Garey and Leuba, 1986; Johnson et al., 1994; Tarpley and Hof et al., 1992, 1995; Glezer et al., 1990, 1992a,b, 1993, Ridgway, 1994; Manger et al., 1998; Marino, 1998). Fur- 1998), cortical surface morphology (Jacobs et al., 1979; thermore, with the exception of Morgane et al. (1980), Morgane et al., 1980; Haug, 1987), noncortical structures Ridgway and Brownson (1984), Haug (1987), and Tarpley ANATOMY OF THE WHITE WHALE BRAIN 431 Fig. 2. Three-dimensional digital reconstructions of the whole brain and resectioning to produce “virtual” horizontal sections. Fig. 3. Three-dimensional digital reconstructions of the whole brain and resectioning to produce “virtual” sagittal sections. and Ridgway (1994) there are no systematic anatomical their precise spatial interrelationships, which is difficult descriptions of whole cetacean brains and substructures to accomplish after the spatial distortions often accompa- at the qualitative level. There currently exists no compre- nying histological processing. This study presents an an- hensive cetacean neuroanatomical atlas either in paper or atomically-labeled three-dimensional atlas, created from electronic format on which to base studies of cetacean MRI images, of the brain of one of the most behaviorally brain organization and function. This situation is mainly studied odontocetes, the white whale (Delphinapterus leu- due to the time and practicality associated with the prep- cas). aration of such large brain specimens. Magnetic resonance MATERIALS AND METHODS imaging (MRI) offers a means of observing the internal structure of the brain where traditional procedures of Specimen embedding, sectioning, staining, mounting, and micro- The specimen is the postmortem brain, fixed in 10% scopic examination of thousands of sections are not prac- buffered formalin, of an adult female white whale (Delphi- tical. Furthermore internal structures can be analyzed in napterus leucas) who died of natural causes. The whale 432 MARINO ET AL. Figure 4. ANATOMY OF THE WHITE WHALE BRAIN 433 had been involved in several behavioral studies including studies of its hearing (Awbrey et al., 1988). At death, the brain was extracted from the skull, weighed, and placed in neutral buffered formalin for 4 years before scanning. Fresh brain weight was 1,871 g. Fixed brain weight was 1,755 g at the time of scanning. Magnetic Resonance Imaging The brain was removed from the fluid and placed in a head coil ventral side down. Images of the entire brain were acquired in the coronal plane at 119 antero-posterior levels with a 1.5 T Siemens scanner (slice thickness ϭ 1.3 mm, slice interval ϭ 1.3 mm, isotropic 1 mm voxels, MP- RAGE sequence, field of view ϭ 240 mm, matrix ϭ 256 ϫ 256). The scanning was done by Richard Buxton, PhD at the University of California, San Diego. Three-Dimensional Reconstruction and Reformatting Computer-generated three-dimensional reconstruction images were created by Timothy L. Murphy, using the software programs VoxelView and VoxelMath programs (Vital Images, Inc.) at the Laser Scanning Microscopy Laboratory at Michigan State University, Joanne Whal- lon, Director. The 3D rendered model, wherein details of internal and external morphology are represented in three-dimensional space, was then digitally resectioned in orthogonal planes to produce corresponding 0.9375 mm- thick “virtual” sections in the horizontal (163 “virtual” sections) and sagittal (236 “virtual” sections) planes. Anatomical Labeling and Nomenclature All identifiable anatomical structures of the white whale brain were labeled in the originally-acquired coro- nal plane images as well as in the images from the “vir- tual” sectioned brain in the sagittal and horizontal planes. The nomenclature used is from Morgane et al. (1980). As a guide to the identification of structures, the MRI scans and the sections from the three-dimensional reconstruc- tion of the whale brain were compared with the few pub- lished illustrations (or images of real stained) sections through the white whale brain and photographs of the whole brain (Yablokov et al., 1964; Morgane et al., 1980). They were also compared with similar MRI scans and “virtual” sections and three-dimensional reconstructions from the scans of brains of bottlenose dolphins (Tursiops truncatus) (Morgane et al., 1980). All were compared with complete alternate series of sections from brains of bottle- nose dolphins, stained, respectively, for cell bodies (Nissl method), and for myelinated fibers in the same three or- thogonal planes (coronal, sagittal, and horizontal). These stained section series are from the Yakovlev-Haleem col- lection at the National Museum of Health and Medicine and the Welker collection at the University of Wisconsin- Madison. RESULTS Three-Dimensional Reconstruction Three-dimensional reconstructions of the white whale’s whole brain were produced from the original scans in the Fig. 4. Rostral-to-caudal sequence of originally-acquired 1.3 mm-thick coronal brain sections in 22 mm intervals and labeled schematic illus- trations of each section. 434 MARINO ET AL. Figure 5. ANATOMY OF THE WHITE WHALE BRAIN 435 coronal plane. Figure 1 displays an image (or view) of the posterior-ventral surface of a computer-generated three- dimensional reconstruction of the whole brain and a la- beled illustration of the image. Figures 2 and
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