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Neuroanatomy and Volumes of Brain Structures of a Live California Sea Lion (Zalophus californianus) From Magnetic Resonance Images.

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THE ANATOMICAL RECORD 292:1523–1547 (2009)
Neuroanatomy and Volumes of Brain
Structures of a Live California Sea Lion
(Zalophus californianus) From Magnetic
Resonance Images
ERIC W. MONTIE,1* NICOLA PUSSINI,2 GERALD E. SCHNEIDER,3
THOMAS W.K. BATTEY,4 SOPHIE DENNISON,2,5 JEROME BARAKOS,6
2
AND FRANCES GULLAND
1
College of Marine Science, University of South Florida, Florida
2
The Marine Mammal Center, Sausalito, California
3
Department of Brain and Cognitive Sciences, MIT, Cambridge, Massachusetts
4
Eckerd College, Galbraith Marine Science Center, St. Petersburg, Florida
5
School of Veterinary Medicine, University of Wisconsin, Madison, Wisconsin
6
California Pacific Medical Center, University of California, San Francisco, California
ABSTRACT
The California sea lion (Zalophus californianus) has been a focal point
for sensory, communication, cognition, and neurological disease studies in
marine mammals. However, as a scientific community, we lack a noninvasive approach to investigate the anatomy and size of brain structures in
this species and other free-ranging, live marine mammals. In this article,
we provide the first anatomically labeled, magnetic resonance imagingbased atlas derived from a live marine mammal, the California sea lion.
The brain of the California seal lion contained more secondary gyri and
sulci than the brains of terrestrial carnivores. The olfactory bulb was present but small. The hippocampus of the California sea lion was found
mostly in the ventral position with very little extension dorsally, quite
unlike the canids and the mustelids, in which the hippocampus is present
in the ventral position but extends dorsally above the thalamus. In contrast to the canids and the mustelids, the pineal gland of the California
sea lion was strikingly large. In addition, we report three-dimensional
reconstructions and volumes of cerebrospinal fluid, cerebral ventricles,
total white matter (WM), total gray matter (GM), cerebral hemispheres
(WM and GM), cerebellum and brainstem combined (WM and GM), and
hippocampal structures all derived from magnetic resonance images.
These measurements are the first to be determined for any pinniped species. In California sea lions, this approach can be used not only to relate
cognitive and sensory capabilities to brain size but also to investigate the
neurological effects of exposure to neurotoxins such as domoic acid. Anat
C 2009 Wiley-Liss, Inc.
Rec, 292:1523–1547, 2009. V
Grant sponsor: Subaward through the University of
California Davis Wildlife Health Center and the University
Corporation of Atmospheric Research (UCAR) from the
National Oceanic and Atmospheric Administration (NOAA),
U.S.
Department
of
Commerce;
Grant
number:
NA06OAR4310119; Grant sponsors: The Marine Mammal
Center, the US National Marine Fisheries Service, and Dr.
David Mann (College of Marine Science, University of South
Florida).
C 2009 WILEY-LISS, INC.
V
*Correspondence to: Eric W. Montie, College of Marine Science, University of South Florida, 140 Seventh Avenue South,
KRC 2107, St. Petersburg, FL 33701.
E-mail: emontie@marine.usf.edu
Received 26 March 2009; Accepted 28 April 2009
DOI 10.1002/ar.20937
Published online in Wiley InterScience (www.interscience.wiley.
com).
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MONTIE ET AL.
Key words: California sea lion; Zalophus californianus; pinniped; magnetic resonance imaging; brain;
hippocampus; MRI
INTRODUCTION
Since the 1960s, the California sea lion (Zalophus californianus) has been a model organism for sensory, communication, and cognition studies in marine mammals.
Behavioral research on this animal has focused on visual
acuity and discrimination between objects (Kastak and
Schusterman, 2002a; Schusterman et al., 1965; Schusterman and Balliet, 1970), hearing sensitivity (Schusterman, 1974; Reichmuth et al., 2007), vocalizations and
communication (Schusterman et al., 1966; Schusterman
and Balliet, 1969; Hanggi and Schusterman, 1990;
Gisiner and Schusterman, 1991), and memory (Schusterman et al., 1993; Kastak and Schusterman, 2002a).
However, to the best of our knowledge, no formal studies
have focused on the anatomy and size of brain structures in this species.
In the wild, California sea lions can be exposed to
domoic acid (DA), a natural marine neurotoxin produced
by diatoms belonging to the Pseudo-nitzschia genus. DA
acts as an excitotoxin by binding to the a-amino-5hydroxy-3-methyl-4-isoxazole propionic acid and kainate
subclasses of neuronal glutamate ionotropic receptors
(Jeffrey et al., 2004). This binding causes massive cell
depolarization, resulting in dysfunction and death of
cells expressing these receptors (Olney et al., 1979). In
1998, more than 400 sea lions were exposed to DA
through contaminated prey (Scholin et al., 2000). Sea
lions that died acutely and contained detectable levels of
DA in blood and urine exhibited lesions in the limbic
system (Scholin et al., 2000). These lesions were characterized by neuronal necrosis in the hippocampal formation, specifically granule cells in the dentate gyrus and
pyramidal cells in sectors CA4, CA3, and CA1 of the
cornu ammonis (Silvagni et al., 2005).
A second novel neurological syndrome has been identified in California sea lions associated with chronic exposure to sublethal levels of DA (Goldstein et al., 2008).
Sea lions examined alive by magnetic resonance imaging
(MRI) exhibited varying degrees of hippocampal atrophy,
thinning of the parahippocampal gyrus, and increases in
the size of the temporal horn of the lateral ventricle
(Goldstein et al., 2008). This examination was based on
subjective analysis and not on volumetric measurements. Now, there is concern that low levels of DA exposure in the developing fetus and neonate, via
concentration in the amniotic fluid and mammary
glands, respectively, may cause subtle changes in the
brain that may result in long-term cognitive impairment
(as reviewed by Ramsdell and Zabka, 2008). As humans
can also be exposed to DA in seafood, there is a need to
understand the range of effects that DA may have on
naturally exposed mammals, so effects on humans can
be predicted and prevented.
With the widespread exposure of wild sea lions to DA,
there is a need to learn more about the normal brain of
the California sea lion to accurately identify changes in
the brain due to DA toxicity. MRI has been used recently
to study the anatomy of cetacean brains that were
removed from the skull and formalin fixed (Marino
et al., 2001a,b,c, 2003a,b, 2004a,b) and that were freshly
intact within the skull and attached to the body (Montie
et al., 2007, 2008). For the Atlantic white-sided dolphin
(Lagenorhynchus acutus), MRI has been used to acquire
images of the brain to calculate the volumes of white
matter (WM), gray matter (GM), cerebellum WM and
GM, and the hippocampus at different developmental
stages (Montie et al., 2008). Using these methods, MRI
provides a means to evaluate normal brain structure
and determine the size of brain regions in live California
sea lions. This approach would be a valuable tool in
assessing the effects of DA neurotoxicity in exposed
animals.
Our goal in this study was to create a neuroanatomical atlas and establish a quantitative approach to determine the size of brain structures from MR images of a
live California sea lion. Specifically, the objectives were
to (a) present an anatomically labeled MRI-based atlas
of a neurologically normal brain; (b) provide detailed
labeling of hippocampal structures; (c) determine the
WM and GM volumes of the total brain, cerebellum and
brainstem combined, and cerebral hemispheres; and (d)
determine the volumes of the left and right hippocampus
and associated structures.
MATERIALS AND METHODS
Animal Information
The female California sea lion used in this study
(Accession number ¼ CSL7775; Name ¼ ‘‘Kirina’’) was
rescued on 25 July, 2008 by the Marine Mammal Center,
Sausalito, CA from Pico Point, San Simeon, CA
(35 360 46.799400 N, 121 90 7.200 W) due to a fractured
right hind flipper. Hematological and serum biochemical
parameters were within the normal range for this species, other than an elevated white blood cell count. A
neurological assessment (posture, mentation, body movements other than use of the right hind flipper, cranial
nerve reflexes, and responsiveness to audible stimuli
and visual approach) appeared normal. At the time of
MRI, the body length was 117 cm, and the weight was
34.5 kg. These measurements along with the stage of
tooth development indicated that the animal was
approximately 1 year old (Greig et al., 2005). Radiography and MRI were used to evaluate the flipper and
brain of the sea lion to determine its prognosis. MR examination did not reveal any brain pathologies; the
brain appeared grossly normal.
Magnetic Resonance Data Acquisition
Radiographs of the whole body nullified any suspicion
of metallic foreign bodies present in the animal. The animal was imaged at IAMs Pet Imaging Center, San Francisco, CA, following anesthesia with isoflurane. MRI
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
TABLE 1. List of anatomical nomenclature
Nomenclature used in
sea lion atlas
Accumbens nucleus
Alveus
Amygdala
Anterior olfactory nucleus
Basilar artery
Calcarine sulcus
Caudal cerebellar peduncle
Caudal cerebral artery
Caudal colliculus
Caudal commissure
Caudate nucleus
Central canal
Cerebellum (hemisphere)
Cerebellum (nodulus)
Cerebellum (vermis)
Cerebral falx
Choroid plexus
Cingulate gyrus
Cingulate sulcus
Cochlea
Collateral sulcus
Cornu ammonis
Coronal gyrus
Coronal sulcus
Corpus callosum (body)
Corpus callosum (genu)
Corpus callosum (splenium)
Dentate gyrus
Dentate nucleus
Dorsal venous sinus
External capsule
Fimbria
Fornix
Interpeduncular Fossa
Fourth ventricle
Fourth ventricle (lateral recess)
Frontal gyrus
Frontal lobe
Globus pallidus
Habenular nucleus
Hippocampal sulcus
Hippocampus
Horizontal sulcus
Hypothalamus
Infundibulum
Internal capsule
Interventricular foramen
Lateral geniculate body
Lateral lemniscus
Lateral ventricle (caudal horn)
Lateral ventricle (central)
Lateral ventricle (rostral horn)
Lateral ventricle (ventral horn)
Longitudinal cerebral fissure
Mammillary body
Medial geniculate body
Medulla oblongata
Mesencephalic aqueduct
Middle cerebellar peduncle
Obex
Occipital lobe
Olfactory bulb
Alternate names
Nucleus accumbens1
Alveus hippocampi1
Corpus amygdaloideum1
Nucleus olfactorius anterior1
Arteriae basilaris1
Sulcus calcarinus1
Pedunculus cerebellaris caudalis1
Arteriae cerebri caudalis1, posterior cerebral artery2
Colliculus caudalis1, inferior colliculus2
Commisura caudalis1, commisura posterior3
Nucleus caudatus1
Canalis centralis1
Hemispherium cerebelli1
Falx cerebri1
Plexus choroideus1
Gyrus cinguli1
Hippocampus proper2; Ammon’s horn2; CA1, CA2,
CA3, CA4 2
Gyrus coronalis1
Sulcus coronalis1
Truncus corporis callosi1
Genu corporis callosi1
Splenium corporis callosi1
Gyrus dentatus1
Nucleus dentatus1
Capsula externa1
Fimbria fornicus3
Fossa interpeduncularis1
Ventriculus quartus1
Recessus lateralis ventriculi quarti1
Gyrus frontalis1
Pallidum1
Nucleus habenulares1
Sulcus hippocampi1
Sulci cerebelli1
Capsula interna1
Foramen interventriculare1
Corpus geniculatum laterale1
Lemniscus lateralis1
Ventriculus lateralis1, lateral ventricle (posterior
or occipital horn)2
Ventriculus lateralis1
Ventriculus lateralis1, lateral ventricle (anterior
or frontal horn)2
Ventriculus lateralis1, lateral ventricle (inferior
or temporal horn)2
Fissura longitudinalis cerebri1
Corpus mamillare1
Corpus geniculatum mediale1
Pyramis1
Aqueductus mesencephali1
Pedunculus cerebellaris medius1
Bulbus olfactorius1
1525
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MONTIE ET AL.
TABLE 1. List of anatomical nomenclature (continued)
Nomenclature used in
sea lion atlas
Olfactory peduncle
Olfactory tubercle
Optic chiasm
Optic nerve
Parahippocampal gyrus
Periaqueductal gray matter
Pineal gland
Pituitary gland
Pons
Precommisural septal fibers
Presylvian sulcus
Proreal gyrus
Pulvinar
Putamen
Pyramidal tract
Reticular formation
Rostral cerebellar artery
Rostral cerebellar peduncle
Rostral cerebral artery
Rostral colliculus
Rostral commissure
Rostral rhinal fissure
Septal nucleus
Septum
Spinal cord
Straight gyrus
Stria medullaris
Subiculum
Sulcus cruciatus
Suprasylvian gyrus
Sylvian fissure
Temporal lobe
Tentorium cerebelli
Thalamus
Third ventricle
Transverse pontine fibers
Trigeminal ganglion
Trigeminal nerve
Trigeminal nucleus
Turbinate bones
Vestibulocochlear nerve
Alternate names
Pedunculus olfactorius1, olfactory tract2
Tuberculum olfactorium1
Chiasma opticum1
Nervi opticus1, cranial nerve II2
Gyrus parahippocampalis1, lobus piriformis3
Substantia grisea centralis1
Glandula pinealis1
Hypophysis or Glandula pituitaria1
Commisura fornicis dorsalis1, fibrae
precommissurales septi3
Sulcus presylvius1
Gyrus proreus1
Tractus pyramidalis1
Formatio reticularis1
Arteriae cerebelli rostralis1, superior
cerebellar artery2
Pedunculus cerebellaris rostralis1
Arteriae cerebri rostrallis1, anterior cerebral artery2
Colliculus rostralis1, superior colliculus2
Commisura rostralis1, commisura anterior3
Fissura rhinalis rostralis1
Nucleus septalis1
Septum telencephali1
Gyrus rectus3
Subiculum1
Sulcus cruciatus1
Gyrus suprasylvius1
Fissura sylvia or lateralis cerebri1
Ventriculus tertius1
Fibrae pontis transversae1
Ganglion trigeminale1
Nervi trigeminus1, cranial nerve V2
Ethmoturbinalia1
Nervi vestibulocochlearis1, cranial nerve VIII2
1
Nomenclature reported in Nomina Anatomica Veterinaria (fifth edition).
Nomenclature by Nolte and Angevine (2000).
3
Nomenclature by Dua-Sharma et al. (1970).
2
scanning of the brain was completed with a 1.5-T Siemens Magnetom Symphony scanner (Siemens, Munich,
Germany) equipped with a CP Extremity Coil. Following
the localizer scan, T1-weighted images in the sagittal
plane were acquired using a spoiled gradient echo
(FLASH) sequence with the following parameters: TR ¼
22 ms; TE ¼ 10 ms; FOV ¼ 200 200 mm; slice thickness ¼ 1 mm; and voxel size ¼ 0.3 0.3 1 mm. Twodimensional proton density (PD) and T2-weighted
images in the transverse plane were acquired using a
turbo spin-echo (TSE) sequence with the following parameters: TR ¼ 3650 ms and TE ¼ 14/98 ms for PD and
T2, respectively; slice thickness ¼ 2.5 mm; FOV ¼ 150 150 mm; and voxel size ¼ 0.3 0.3 2.5 mm. Additionally, two-dimensional PD- and T2-weighted images in
the oblique plane (i.e., perpendicular to the long axis of
the sylvian fissure and temporal lobe) were acquired
using a TSE sequence with the following parameters:
TR ¼ 5470 ms and TE ¼ 14/98 ms for PD and T2,
respectively; slice thickness ¼ 2.5 mm; FOV ¼ 160 160 mm; and voxel size ¼ 0.3 0.3 2.5 mm. The
oblique orientation was selected to optimize viewing of
the hippocampus, as previously described (Goldstein
et al., 2008).
After radiography and MR examination, the animal
was euthanized because of poor prognosis for rehabilitation and release due to the severity of osteomyelitis in
the hind flipper. A necropsy was completed. The brain
was removed, weighed, and archived whole in 10% neutral buffered formalin.
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1527
Fig. 1. 3D reconstruction of the brain surface of a California sea
lion, in which MRI was performed live. (A) Side view of brain reconstruction with parasagittal section through surrounding head structures. (B) Reconstruction with head structures removed. Orange,
cerebral hemisphere gray matter (GM); white, cerebellum; red, spinal
cord; aqua blue, olfactory bulb and tract; purple, optic nerves. Scale
bars ¼ 10 cm. (C) Side view of brain removed and fixed in formalin.
Scale bar ¼ 1 cm. Yellow arrows demarcate the position of the Sylvian
fissure.
Anatomic Labeling and Nomenclature
eFilm Lite 2.1.2 (Merge Healthcare, Milwaukee, WI) from
the Digital Imaging and Communication in Medicine
(DICOM) files saved during the TSE sequences. T2weighted images were used in the label schematics because
these images are very sensitive to minute changes in water
concentration and are therefore useful in illustrating pathology within the brain. The oblique T2-weighted images
were selected for the hippocampal atlas because these
images were exceptional in defining hippocampal anatomy,
as previously described (Goldstein et al., 2008).
Anatomical structures were identified using the brain
atlas of the domestic dog (Beagle, Canis familiaris) (DuaSharma et al., 1970) and human (Nolte and Angevine,
2000) and labeled using nomenclature adopted from the
English translation of Nomina Anatomica Veterinaria
(ICVGAN, 2005) (Table 1). Comparisons of the California
sea lion brain to other species in the Order Carnivora
were made using the Comparative Mammalian Brain Collection website (http://www.brainmuseum.org/index.html)
prepared by the University of Wisconsin, Michigan State
University and the National Museum of Health and Medicine (Welker et al., 2009). Segmentation (i.e., assigning
pixels to particular structures) and three-dimensional
(3D) reconstructions of the brain surface were performed
using the software program AMIRA 4.1.1 (Mercury Computer Systems, San Diego, CA). To create a 3D reconstruction of the brain surface, the pixels in the native (i.e., no
image processing) T1-weighted images from the FLASH
sequence were selected manually and defined as cerebrum, cerebellum, spinal cord, olfactory bulb and tract,
and optic nerves.
The atlases of the brain and hippocampus of the
California sea lion were constructed from native (i.e., no
image processing) transverse and oblique T2-weighted
images, respectively. These images were created using
Volume Analysis of Brain Structures
Visualization of MR images was completed first on the
MRI unit. Post-processing, segmentation, 3D reconstructions, and volume analysis were also performed using
the software program AMIRA 4.1.1 (Mercury Computer
Systems, San Diego, CA). 3D reconstructions and volumes of brain structures that were determined included
whole brain; cerebrospinal fluid (CSF) of the total, left,
and right brain; CSF of the total, left, and right cerebral
ventricles; GM and WM of the entire brain; GM and
WM of the total, left, and right cerebral hemispheres;
and GM and WM of the cerebellum including the brainstem. Volumes of the left and right hippocampus and
associated structures that were determined included
1528
MONTIE ET AL.
Fig. 2. (Legend on page 1537)
Fig. 3. (Legend on page 1537)
lateral ventricle (ventral horn); hippocampal sulcus; hippocampus and parahippocampal gyrus combined; hippocampus alone; parahippocampal gyrus alone; and
parahippocampal gyrus WM and GM. The WM of the
parahippocampal gyrus most likely contained fibers of
the subiculum because of the inability to identify boundaries between WM of the parahippocampal gyrus and
WM of the subiculum. Segmenting brain structures, creating 3D reconstructions, and volume analysis used
methods similar to those described by Montie et al.
(2008) with modifications explained below.
Brain CSF, GM, and WM. To determine the volumes of brain structures, a brain surface mask created
from the native T2-weighted transverse images was produced to determine edges for digital removal of nearby
blubber, muscle, skull, and other head structures. The
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1529
Fig. 4. (Legend on page 1537)
Fig. 5. (Legend on page 1537)
mask was constructed by manually tracing the surface
of the brain and deleting all pixels outside this trace for
each MR image. The whole brain volume was calculated
by integrating the area of the selected tissue for each
slice of the brain surface mask. The caudal boundary of
the brain was defined by the caudal aspect of the foramen magnum. Virtual brain weight was calculated by
multiplying the total brain segmented volume by the
assumed specific gravity of brain tissue, 1.036 g/cm3
(Stephan et al., 1981).
Total brain CSF volumes were determined by threshold segmentation of the brain surface mask (obtained
from the native T2-weighted transverse images) followed
by manual editing of each slice. Specifically, this procedure involved thresholding for signal intensity ranges
that captured the boundaries of brain CSF followed by
visual inspection and manual editing to ensure that CSF
was properly defined. From this segmentation, pixels
representing CSF of the left and right hemispheres were
manually selected and defined as a new label field (i.e.,
1530
MONTIE ET AL.
Fig. 6. (Legend on page 1537)
Fig. 7. (Legend on page 1537)
a set of images where pixels are selected to represent
different anatomical structures). Pixels of the left and
right ventricular system that captured the lateral, third,
and fourth ventricles were manually selected and
defined as another label field. The volumes of these
structures (i.e., total CSF, left and right CSF, total ventricles, left and right ventricles) were determined three
separate times. The mean volume (cm3) and standard
deviation of these structures were reported.
Total GM and WM volumes were determined by a
combination of manual and threshold segmentation of
processed, transverse PD-weighted images. Processing
involved deleting the pixels outside the brain surface
mask and deleting the pixels of each CSF label field
from the native PD-weighted transverse images. From
the processed PD-weighted images, the segmentation
procedure involved thresholding for signal intensity
ranges that captured the boundaries of GM and WM
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1531
Fig. 8. (Legend on page 1537)
Fig. 9. (Legend on page 1537)
followed by visual inspection and manual editing to
ensure that GM and WM were properly defined. The volume of total GM and WM was then determined. From
this segmentation, pixels representing cerebral GM and
WM and pixels representing cerebellum and brainstem
GM and WM were manually selected and defined as a
new label field. The volumes of total cerebral GM and
WM and cerebellum plus brainstem GM and WM were
determined. The pixels defining GM and WM of the cerebellum were combined with the pixels representing GM
and WM of the brainstem because the boundaries of the
cerebellum and brainstem were not easily recognized.
Pixels defining the left and right cerebral GM and WM
were manually selected and the volumes of these structures determined. For each structure, volumes were
determined three times. The mean volume (cm3) and
standard deviation of these structures were reported.
Hippocampus. Volumes of the left and right hippocampus and associated structures were determined by
1532
MONTIE ET AL.
Fig. 10. (Legend on page 1537)
Fig. 11. (Legend on page 1537)
manual segmentation of native, oblique T2-weighted
images. The T2-weighted images were used because they
were better at highlighting fluid structures surrounding
the hippocampus compared with the PD images. These
fluid structures served as boundaries of the hippocampus and were defined by higher signal intensities. The
atlas by Dua-Sharma et al. (1970) and the hippocampus
atlas we constructed served as guides for segmenting
the left and right hippocampus and associated struc-
tures. For these volume calculations, the various structures of the hippocampal formation (i.e., subiculum,
cornu ammonis, and the dentate gyrus) could not be
adequately distinguished. These brain regions and the
fimbria and alveus were collectively grouped and
referred to as the hippocampus. Structure volumes were
determined three times, separately. The mean volume
(mm3) and standard deviation of these structures were
reported.
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1533
Fig. 12. (Legend on page 1537)
Fig. 13. (Legend on page 1537)
The percentage of brain occupied by the left or right
hippocampal structure was calculated by dividing that
structure’s volume (i.e., from the native oblique T2weighted images) by the sum of the WM and GM volumes of the whole brain (i.e., from the processed PDweighted images) multiplied by 100. The percentage of
cerebral hemisphere occupied by the left or right hippocampal structure was calculated by dividing the structure volume (i.e., from native T2 weighted images) by
the sum of the left or right cerebral WM and GM vol-
umes (i.e., from processed PD weighted images) multiplied by 100.
RESULTS AND DISCUSSION
3D Reconstruction of the Brain Surface from
Magnetic Resonance Images
Comparing the 3D reconstruction of the California
sea lion brain to photographs of formalin-fixed brains
of other mammals (i.e., from the Comparative
1534
MONTIE ET AL.
Fig. 14. (Legend on page 1537)
Fig. 15. (Legend on page 1537)
Mammalian
Brain
Collection
website,
http://
www.brainmuseum.org/index.html) showed the resemblance of the sea lion brain to the brains of other species belonging to the Order Carnivora, specifically
carnivores within the Suborder Caniformia (Fig. 1).
The California sea lion brain was similar in shape to
representative species in the Family Canidae [e.g., the
domestic beagle (Canis familiaris), the wolf (Canis
lupus), and the coyote (Canis latrans)]; the Family
Ursidae [e.g., the polar bear (Ursus maritimus)]; and
the Family Mustelidae [e.g., the American mink (Neovison vison) and the American badger (Taxidea taxus)].
Compared with the canids, ursids, and mustelids, the
California sea lion brain was expanded laterally, with
large frontal, temporal, and occipital lobes. Qualitative
comparisons of the degree of neocortical folding (or gyrification) among these carnivores indicated that the
brain of the California sea lion contained more secondary folds and sulci than the American mink, the American badger, the domestic beagle, the wolf, the coyote,
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1535
Fig. 16. (Legend on page 1537)
Fig. 17. (Legend on page 1537)
and the polar bear. In addition, the pattern of folds
and fissures in the sea lion brain was very different
from these carnivores. For example, the Sylvian fissure
in the sea lion brain was perpendicular to the ventral
surface of the brain, whereas in the domestic dog, the
sulcus was obtuse (135 ) to the ventral surface. The
Sylvian fissure in the sea lion also extended deeper
into the brain towards the longitudinal cerebral fissure
compared with the shallower fissures in the domestic
dog.
The increase in gyri and sulci in the California sea
lion compared with canids and mustelids may be best
explained by the larger brain size in the sea lion. Neocortical folding has been shown to correlate with brain
size in large-brained mammals in many different lineages, as reviewed by Striedter (2005). It has been speculated that the neocortex tends to fold in large brains
because the most efficient way to increase the area of
the neocortex without dramatically increasing neocortex
thickness is for the neocortex to fold inward [as reviewed
1536
MONTIE ET AL.
Fig. 18. (Legend on page 1537)
Fig. 19. (Legend on page 1537)
by Striedter (2005)]. If the neocortex were to have ballooned outward, the expansion without this folding
would have yielded very large heads and long intracortical connections, both unfavorable factors during natural
selection [as reviewed by Striedter (2005)].
Neuroanatomical Atlas from Magnetic
Resonance Images
Figures 2–21 display a rostral-to-caudal sequence of T2weighted, 2.5 mm-thick transverse MR brain sections at 5
mm intervals. Panels A display a sagittal section showing
the orientation and level at which the T2 section was
taken; Panels B illustrate the position of the brain in the
transverse plane relative to surrounding head structures
of the T2-weighted image; panels C show labeled versions
of each brain section. The right side of the images corresponds to the left side of the brain, which is the traditional
method in showing radiological images. These figures
demonstrate undisturbed spatial relationships among
brain structures and surrounding head anatomy obtainable by MR imaging of live animals.
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1537
Fig. 20. (Legend on page 1537)
Fig. 21. Fig 2-21. Rostral-to-caudal sequence of transverse T2weighted images of the brain of a California sea lion imaged live. (A)
Sagittal MR images illustrating the orientation of the section. Dotted
lines represent the plane of section. Scale bar ¼ 10 cm. (B) Native T2-
weighted 2.5 mm-thick transverse MR brain sections at 5 mm intervals with surrounding head structure. Scale bar ¼ 5 cm. (C) Labeled
brain section with head structures removed.
Figures 22–35 display a ventral-to-dorsal sequence of
T2-weighted, 2.5-mm thick oblique MR brain sections at
2.5 mm intervals of the hippocampal region. Panels A display a sagittal section showing the orientation and level
at which the T2 section was taken; panels B illustrate the
position of the brain in the oblique plane relative to sur-
rounding head structures of the T2-weighted image; panels C show labeled versions of each brain section. The
right side of the images corresponds to the left side of the
brain. The images obtained in the oblique plane provided
a better view of the hippocampus compared with the
images obtained in the transverse plane.
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MONTIE ET AL.
Fig. 22. (Legend on page 1544)
Fig. 23. (Legend on page 1544)
Telencephalon. The MR images illustrate distinguishing features of the California sea lion telencephalon. The size of the olfactory bulb relative to the brain is
small (Figs. 2C–3C); comparisons indicated that the bulb
in canids, ursids, and mustelids are larger. The decrease
in size of this brain structure in California sea lions may
be related to the possibility that sea lions rely less on olfactory signals to detect prey and predators than terrestrial carnivores. It is very possible that pinnipeds do not
have active olfaction underwater (Denhardt, 2002).
The neocortex was highly convoluted and contained
many secondary gyri and sulci that were not identifiable
using the domestic dog atlas (Figs. 2C–21C). The suprasylvian gyrus was expanded laterally (Figs. 5C, 6C),
more so than the gyrus of the domestic dog. Despite the
large hemispheres, the corpus callosum appears to be
small (Figs. 8C–13C).
Structures of the basal ganglia (i.e., the caudate nucleus, the putamen, and the globus pallidus) were identified (Figs. 7C–12C). Interestingly, the caudate nucleus in
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1539
Fig. 24. (Legend on page 1544)
Fig. 25. (Legend on page 1544)
the California sea lion seems to have a very small tail.
The putamen was difficult to recognize and seemed to be
mixed with fiber bundles.
The amygdala was evident in the rostral portion of the
temporal lobes (Figs. 10C, 22C), whereas the hippocampus was located near the center of the sections in the
medial wall of the temporal lobes (Figs. 11C–13C, 23C–
33C). The boundaries of the hippocampus were best
observed in native T2-weighted images rather than PD-
weighted images. This finding can be best explained by
the CSF surrounding the hippocampus, as observed by
the hyperintensity of the ventral horns of the lateral
ventricles (lateral and dorsal borders) (Figs. 11C–13C,
23C–33C) and the hyperintensity of the hippocampal
sulcus (medial border) (Figs. 11C–12C, 22C–29C). The
structures of the hippocampal formation were best
visualized in the oblique T2-weighted images (Figs.
23C–33C). These structures included the cornu ammonis
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MONTIE ET AL.
Fig. 26. (Legend on page 1544)
Fig. 27. (Legend on page 1544)
or hippocampus proper (Figs. 23C–33C), the subiculum
(Figs. 24C–29C), and the dentate gyrus (Figs. 26C–30C).
The small size of the dentate gyrus made its identification very difficult in some of the sections. WM tracts of
the hippocampus, the alveus and fimbria, were also
identified (Figs. 24C–32C). The parahippocampal gyrus
was easily recognized in the MR images (Figs. 11C–13C,
23C–33C).
One very interesting finding was that the California
sea lion hippocampus was found mostly in the ventral
position with very little extension dorsally (Figs. 11C–
13C, 23C–33C). However, in canids and mustelids, the
hippocampus is present in the ventral position but also
extends dorsally above the thalamus (Dua-Sharma
et al., 1970; Welker et al., 2009).
Diencephalon. The MR images revealed a large diencephalon in the California sea lion. The hypothalamus
(Figs. 10C–11C) and thalamus (Figs. 10C–14C) were
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1541
Fig. 28. (Legend on page 1544)
Fig. 29. (Legend on page 1544)
easily recognized in the MR images. The optic nerves
(Figs. 5C–8C), optic chiasm (Fig. 9C), and pituitary
gland (Figs. 10C–12C) were also observed. The mammillary body was visualized, protruding downward towards
the pituitary gland (Fig. 11C). The pineal gland was
very prominent, located in the midline above the caudal
commissure (Fig. 13C). This finding was expected, as the
pineal gland is known to be exceptionally large in pinnipeds (Cuello and Tramezzin, 1969; Turner, 1888). The
habenular nucleus was also located just underneath the
pineal gland (one on each side) (Fig. 12C).
Mesencephalon. The rostral colliculus (i.e., superior
colliculus in bipeds) was easily identified, as was the
caudal colliculus (i.e., inferior colliculus in bipeds) (Fig.
14B). Neither of these structures appeared to be particularly enlarged.
1542
MONTIE ET AL.
Fig. 30. (Legend on page 1544)
Fig. 31. (Legend on page 1544)
Rhombencephalon. The MR images showed typical
characteristics of the carnivore metencephalon and myelencephalon. Auditory pathways were observed, including the cochlea (Fig. 15C), the vestibulocochlear nerve
(Fig. 15C), and the lateral lemniscus (Fig. 14C). The trigeminal ganglion (Figs. 10C–12C) and trigeminal nerve
(Figs. 13C–15C) were identified, as well as the trigeminal nucleus (Fig. 17C). The cerebellum was large, and
GM and WM were easily distinguishable (Figs. 15C–
21C). Hindbrain structures including the pons (Figs.
13C–15C), reticular formation (Figs. 13C–20C), pyramidal tract (Figs. 16C–17C, 20C–21C), and medulla oblongata were identified (Figs. 20C, 21C).
CSF and Cerebral Ventricles. The three major
processes of the lateral ventricles were easily recognized
including the rostral or frontal horn (Figs. 7C–14C), the
caudal or occipital horn (Fig. 15C), and the ventral or
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
1543
Fig. 32. (Legend on page 1544)
Fig. 33. (Legend on page 1544)
temporal horn (Figs. 11C–14C). The third ventricle
appeared as a thin slit between the two thalami or hypothalami (Figs. 10C–12C). The interventricular foramen
(i.e., a fluid connection where CSF flows from the lateral
ventricles to the third ventricle) was observed (Fig. 11C).
The mesencephalic aqueduct (i.e., a thin, fluid connection where CSF flows from the third to the fourth ventricle) was identified but characterized by a signal void
(Figs. 13C–14C). The lack of CSF signal in the mesencephalic aqueduct represents a flow artifact secondary to
pulsatile CSF flow (Feinberg and Mark, 1987; Malko
et al., 1988; Lisanti et al., 2007). The fourth ventricle
was visualized as a tent-like structure just dorsal of the
reticular formation and ended at the obex (Figs. 16C–
19C). The lateral recess of the fourth ventricle (i.e., a
site where CSF leaves the ventricular system and enters
the subarachnoid space) was also observed (Fig. 18C).
The choroid plexus (i.e., vascular tufts responsible for
CSF production) in the lateral ventricles (Figs. 10C–
12C) and the fourth ventricle (Fig. 18C) were recognized.
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MONTIE ET AL.
Fig. 34. (Legend on page 1544)
Fig. 35. Fig. 22-35. Ventral-to-dorsal sequence of oblique T2weighted images of the hippocampal region of a California sea lion
imaged live. A: Sagittal MR images illustrating the orientation of the
section, which was perpendicular to the temporal lobe and sylvian fissure. Dotted blue lines represent the plane of section. Scale bar ¼ 7
cm. B: Native T2-weighted 2.5-mm thick oblique MR brain sections at
2.5-mm intervals with surrounding head structure. Scale bar ¼ 1 cm.
The dotted rectangle represents the magnified image in panel C. C:
Labeled brain section with head structures removed. Scale bar ¼ 1
cm.
Choroid plexus appears to be present in the third ventricle as well (Fig. 12C).
surface and calculate whole brain volume (Table 2). The
volume of the entire brain was 301.71 cm3, which included
CSF of the subarachnoid space and cerebral ventricles.
The virtual brain weight (calculated by multiplying the
measured volume by the specific gravity of brain tissue)
was 312.6 g. This estimate was very similar to the actual
brain weight measured after fixation (i.e., 306 g).
Volumes of Brain Structures
Brain CSF, GM, and WM. Segmentation of the transverse T2-weighted images was used to delineate the brain
BRAIN MRI OF A LIVE CALIFORNIA SEA LION
The volumes of CSF and cerebral ventricles were
determined from segmentations of the transverse T2weighted images, after digital removal of nearby blubTABLE 2. Brain volumes of the California
sea lion
Structure
Volume (cm3)
Whole brain
Total cerebrospinal fluid
Left cerebrospinal fluid
Right cerebrospinal fluid
Total ventricles
Left ventricles
Right ventricles
Total gray matter
Total white matter
Total cerebral gray matter
Left cerebral gray matter
Right cerebral gray matter
Total cerebral white matter
Left cerebral white matter
Right cerebral white matter
Cerebellum and brainstem gray matter
Cerebellum and brainstem white matter
301.71
38.96 2.08
19.94 1.06
19.02 1.03
7.59 0.12
3.76 0.05
3.83 0.07
164.34 6.57
80.07 2.62
129.39 5.22
64.82 2.84
64.06 2.12
54.42 1.87
27.00 1.12
27.43 0.89
25.65 1.13
34.94 1.45
Fig. 36. 3D reconstructions of brain structures of the California sea
lion, in which MRI was performed live. A: Rostral view of the 3D reconstruction of the brain. Surface of left hemisphere, dark pink; surface of
right hemisphere, light pink; left cerebrospinal fluid (CSF), dark purple;
right CSF, light purple. B: Rostral view of the 3D reconstruction of the
WM, with the GM and exterior CSF removed. The CSF of the third and
lateral ventricles are visible (aqua blue), as well as the left (green) and
right (red) hippocampi. WM of left hemisphere, orange; WM of right
1545
ber, muscle, skull, and other head anatomy (Table 2).
The CSF volumes of the left and right hemispheres were
approximately equal (Table 2). In addition, the CSF volumes in the cerebral ventricles of the left and right
hemispheres were similar (Table 2).
The volumes of GM and WM of the brain were estimated from segmentations of the transverse PDweighted images, after digital removal of nearby blubber, muscle, skull, and other head anatomy and removal
of total CSF (Table 2). The volumes of either the GM or
the WM of the left and right cerebral hemispheres were
approximately equal (Table 2). 3D reconstructions of GM
and CSF of the subarachnoid space of the left and right
hemispheres were constructed (Fig. 36A). The GM and
subarachnoid CSF in the 3D reconstruction were then
removed to reveal the underlying WM of the left and
right hemispheres (Fig. 36B).
Hippocampus. The volumes of the ventral horn of
the lateral ventricles, the hippocampal sulcus, the hippocampus (including alveus and fimbria, dentate gyrus,
cornu ammonis, and subiculum), and the parahippocampal gyrus were determined from segmentations of
oblique T2-weighted images (Table 3). The volumes of
hemisphere, tan; WM of cerebellum and brainstem, yellow. C: Rostral
view of the lateral ventricles and hippocampi, with the WM stripped
away. Lateral ventricles, aqua blue; green, left hippocampus; red, right
hippocampus; white, fimbria; brown, alveus; yellow, fornix; bright pink,
mammillary bodies. D: Rostral view of the hippocampi, with the lateral
ventricles removed. Green, left hippocampus; red, right hippocampus;
white, fimbria; brown, alveus; yellow, fornix; aqua blue, septal nucleus;
bright pink, mammillary bodies. Scale bars ¼ 8 cm.
1546
MONTIE ET AL.
TABLE 3. Volumes of the hippocampus and associated structures in the California sea lion
Volume (mm3)
Structure
Left lateral ventricle (ventral horn)
Right lateral ventricle (ventral horn)
Left hippocampal sulcus
Right hippocampal sulcus
Left hippocampus & parahippocampal gyrus
Right hippocampus & parahippocampal gyrus
Left hippocampus
Right hippocampus
Left parahippocampal gyrus
Left parahippocampal gyrus GM
Left parahippocampal gyrus WM3
Right parahippocampal gyrus
Right parahippocampal gyrus GM
Right parahippocampal gyrus WM3
514.218
492.816
313.788
348.373
2232.157
2265.195
771.286
772.914
1463.475
1112.416
351.058
1492.282
1167.997
324.285
8.753
7.486
5.494
15.542
27.933
45.655
16.381
17.786
27.099
27.978
6.404
39.932
29.068
12.290
% of Brain1
0.913
0.927
0.316
0.316
0.599
0.455
0.144
0.611
0.478
0.133
0.018
0.019
0.011
0.002
0.010
0.008
0.005
0.019
0.013
0.006
% of Cerebral
Hemisphere2
2.432
2.476
0.840
0.845
1.594
1.212
0.382
1.631
1.277
0.355
0.054
0.043
0.033
0.006
0.031
0.023
0.014
0.046
0.031
0.016
Percentage of total brain occupied by the left or right structure ¼ left or right structure volume (from native T2-weighted
oblique images) divided by the white matter (WM) plus gray matter (GM) volumes of the whole brain (from processed PDweighted images) multiplied by 100%.
2
Percentage of left or right cerebral hemisphere occupied by the respective left or right structure ¼ left or right structure
volume (from native T2-weighted oblique images) divided by the respective left or right cerebral WM plus left or right cerebral GM volumes (from processed PD-weighted images) multiplied by 100%.
3
The WM of the parahippocampal gyrus may contain subiculum WM.
1
the left and right hippocampus were approximately
equal (Table 3). In addition, the left and right parahippocampal gyri were approximately equal in volume (Table
3). Both the volumes of the left and right hippocampus
were 0.84% of the volumes of the left and right cerebral
hemispheres (Table 3). Both the volumes of the left and
right parahippocampal gyrus were approximately 1.6%
of the volumes of the left and right cerebral hemispheres
(Table 3). 3D reconstructions of the cerebral ventricles
and their association with the hippocampi were created
(Fig. 36C). The ventricles were then removed to reveal
the underlying hippocampi, fornix, septal nucleus, and
mammillary bodies (Fig. 36D). The 3D reconstruction of
the California sea lion hippocampus revealed its ventral
position with very little extension dorsally (Fig. 36D), as
previously mentioned. In the sea lion, only the fornix
was found above the thalamus. This finding in the sea
lion is different from the domestic dog and the American
mink (see the Comparative Mammalian Brain Collection
by Welker et al. (2009), http://www.brainmuseum.org/);
in these terrestrial relatives, the hippocampus is present
in the ventral position but also extends dorsally above
the thalamus.
on the brain of California sea lions (Silvagni et al., 2005;
Goldstein et al., 2008; as reviewed by Ramsdell and
Zabka, 2008). The MRI atlas presented here of a neurologically normal California sea lion will allow us to better evaluate the hippocampus in the oblique plane and
determine the volumes of brain structures. This
approach will help in deciphering the acute, chronic, and
developmental effects of DA exposure, or exposure to
other pollutants, in wild California sea lions, other marine mammals, and wildlife in general.
ACKNOWLEDGMENTS
CONCLUSIONS
The authors thank all the staff and volunteers at the
Marine Mammal Center, especially Elizabeth Wheeler
for performing the necropsy of this animal. They also
thank Dr. Cheryl Cross for providing gross images of
this California sea lion brain, and Dr. Heather Harris
and Dr. Felicia Nutter for their veterinary assistance.
They thank the University of Wisconsin and Michigan
State Comparative Mammalian Brain Collection, and
the National Museum of Health and Medicine for providing gross and histological images of carnivore brains.
The preparations of those images were funded by the
National Science Foundation, as well as the National
Institutes of Health.
This article presents the first anatomically labeled
MRI-based atlas of a pinniped brain. It is different from
previous MRI-based atlases of marine mammals in that
it was created from imaging a live animal. This study
also presents a quantitative approach to determine the
size of brain structures, such as the hippocampus, from
MR images of live California sea lions.
Live MRI scanning coupled with volumetric analysis
can be used not only as a tool to study brain evolution in
pinnipeds but also to investigate the impacts of biological, chemical, and physical agents on marine mammal
health (Montie, 2006). Of particular concern are the
acute, chronic, and possible developmental effects of DA
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