Structural and functional imaging of bottlenose dolphin (Tursiops truncatus) cranial anatomy
1 BIOMIMETICA, La Mesa, CA 91942, USA
2 Space and Naval Warfare Systems Center, San Diego, CA 92152,
USA
3 School of Medicine, University of California, San Diego, CA 92103,
USA
* Author for correspondence (e-mail: ridgway{at}spawar.navy.mil)
Accepted 22 July 2004
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Summary |
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Key words: CT, PET, SPECT, scan, cranium, hearing, echolocation, lipid density, bottlenose dolphin, Tursiops truncatus
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Introduction |
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Reports on the postmortem investigation of delphinid anatomy date
back to the 18th century (Hunter,
1787), with more comprehensive, multi-species reports on cetacean
cranial anatomy surfacing during the past century (e.g.
Fraser and Purves, 1960
).
These postmortem studies have revealed numerous anatomical variations
on the terrestrial mammal theme that are important to sound generation and
sound reception in an aquatic environment. In delphinids, the fusion of middle
and inner ear into the tympano-periotic complex, the migration of the bullar
complex from the skull, the presence of air sinuses around the bulla
(Dudok van Heel, 1962
;
Fraser and Purves, 1960
;
Ketten, 2000
), the presence of
phonic lips (Cranford, 2000
;
Evans and Prescott, 1962
), an
isovaleric-rich fat body in the forehead known as the melon
(Varanasi et al., 1975
;
Varanasi and Malins, 1971
) and
hollow lower jaws filled with acoustic lipids (Varanasi and Malins,
1970a
,b
)
are a few notable adaptations favoring effective sound utilization in the
ocean. The functional role of these adaptations has been inferred by assessing
the spatial and structural relationship between anatomic components of the
auditory and phonation system (e.g.
Cranford et al., 1996
),
variation in design relative to terrestrial species (e.g.
Dudok van Heel, 1962
;
Norris, 1964
;
Reysenbach de Haan, 1956
), the
physiological response of the system following anatomical manipulation
(McCormick et al., 1970
) and
the biochemical composition of pertinent structures
(Varanasi et al., 1975
). These
inferences, considered in relation to the results of psychoacoustic
experiments (e.g. Brill, 1991
)
and physiological responses to manipulation of the system, form the basis for
our current understanding of delphinid hearing and phonation.
The availability of computed tomography (CT) and magnetic resonance imaging
(MRI) devices has stimulated more investigation to determine relationships
between anatomical structures within the cetacean head by allowing internal
anatomy to be viewed without laborious anatomical dissection. These imaging
modalities have been used with postmortem specimens to study the
brain of the bottlenose dolphin (Tursiops truncatus) and the white
whale (Delphinapterus leucas; Marino et al.,
2001a,b
,c
)
as well as the in situ auditory anatomy and sound-producing
structures of several cetacean species
(Cranford, 1988
;
Cranford et al., 1996
;
Ketten, 1994
;
Ketten and Wartzok, 1990
). As
with necropsy procedures, functional properties of tissues are inferred from
their biochemical composition, morphology and relationship to other tissues.
Unfortunately, postmortem specimens often have to be frozen and then
thawed for scanning, and such freezing and thawing may produce tissue
distortion and permit the draining of fluids into air cavities with the
breakdown of cell membranes and fracturing of capillaries. Furthermore,
changes that begin after death can produce changes in tissue density, gas
bubble generation from bacteria, swelling, rigor mortis and other
distortions (Mackay, 1966
).
Tissue changes following death may therefore lead to spurious conclusions
about tissue function. In vivo measurements made with CT and MRI can
address these issues since such measurements preclude cavity and tissue
deformations and biochemical changes of tissues that follow death.
Functional information of auditory and sound production tissues may be obtained through the use of functional scanning techniques [e.g. single photon emission computed tomography (SPECT) and positron emission tomography (PET)]. By following the distribution of administered radiopharmaceuticals and radionuclides, these scanning techniques allow certain aspects of the physiology of a subject, its organs and tissues, to be observed. In conjunction with in vivo CT and/or MRI measurements, consideration of functional information can provide a more comprehensive understanding of tissue function and structure than can be achieved through postmortem analysis alone.
The current study presents the first CT scans of living bottlenose dolphins and demonstrates the utility of in vivo anatomical analyses. It also presents the first functional scanning of a bottlenose dolphin; both PET and SPECT scans are used to couple information about cranial blood flow and metabolism within the dolphin to anatomical information gained via CT imaging. Results of this study provide new insight into dolphin anatomy and physiology that are pertinent to understanding the role of certain anatomical features in both hearing and echolocation.
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Materials and methods |
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CT scanning
Two dolphins (CIN and WEN) were transported to Vital Imaging of La Jolla,
located approximately 12 miles from their holding enclosures in San Diego Bay.
Each dolphin received 0.30.55 mg kg1 of diazepam to
reduce any anxiety attendant with the scan. X-ray CT was performed using an
electron beam scanner (Imatron, San Francisco, CA, USA) to study the cranial
morphology of the dolphin. Volume acquisition mode was used to image the
entire head. With this mode, X-ray data are acquired helically by rotating an
X-ray source [130 KeV (kilo-electron volts) at 600 MAS (mAmpSec)] collimated
to 3 mm around the object at 100 ms per revolution. Multiple X-ray projections
are then obtained over a 270° arc while the object is translated through
the gantry at 25 mm s1. Each data set (projections acquired
from a single revolution) is used to reconstruct a single cross-sectional
image representing the internal organs located within a transverse plane that
is slightly more than 3 mm thick. Because the object translated 2.5 mm per
revolution, a series of 3 mm-thick images are then made available that are
separated by 2.5 mm. The slight overlap was chosen to produce smooth
three-dimensional (3-D) or multiplanar reconstructions of the imaged region.
Image data were saved in DICOM format and stored to disk until processed.
SPECT
SPECT was used to monitor blood flow in the head tissues of two dolphins.
The SPECT scanner utilizes a gamma camera to acquire gamma rays that are
emitted from radiopharmaceuticals administered to a subject prior to scanning.
Gamma ray photons can be mapped into a two-dimensional (2-D) space; however, a
SPECT camera can acquire images from multiple angles around the patient so
that a 3-D image of the activity can be reconstructed. Technetium
(99mTc) bicisate is a radiopharmaceutical with a high first pass
blood extraction and slow clearance in brain tissue. This property makes it
useful in the mapping of blood flow since the relative image intensity in a
region of brain tissue reflects the underlying blood flow to that region.
99mTc-bicisate is a common diagnostic radiopharmaceutical for
vascular irregularities of the human brain.
Dolphins (WEN and FLP) were administered 99mTc-bicisate (Syncor International Inc., Pasadena, CA, USA) to determine the distribution of blood flow within the brain and other soft tissues of the head. Two hours prior to SPECT imaging, the dolphins received a 1850 MBq intravenous injection of 99mTc-bicisate. Subjects were placed quiescent in a quiet, darkened room for 15 min following injection and were then transported to the Department of Nuclear Medicine at the University of California, San Diego Medical Center. Images were acquired on an ADAC Forte SPECT camera (Milpitas, CA, USA) with the dolphins placed on a specially engineered bed, allowing them to be properly cooled with water. The imaging acquisition consisted of 30 s per stop for a total of 64 angled stops divided between the two imaging heads. This resulted in a total scan time of approximately 32 min. After image reconstruction, the images were converted to the DICOM 3.0 format.
PET
PET was used to estimate the relative metabolism of dolphin cranial
tissues. The PET scanner uses a circular array of detectors to measure photons
produced from positron-emitting radiopharmaceuticals that have been
administered to a subject prior to scanning. As in SPECT imaging, 3-D images
of radiopharmaceutical distributions can be generated where the intensity of
the image represents the relative concentration of the radiopharmaceutical
accumulated in the tissue. 18F-2-fluoro-2-deoxyglucose (FDG) is an
analog of glucose and is often used in PET scanning to estimate glucose uptake
by tissues and is commonly used in the detection of cancerous tissues because
of the relatively higher metabolic rate of cancerous tissue to non-cancerous
tissue.
A single dolphin (WEN) was administered 740 MBq of FDG (Syncor
International Inc.) by intravenous injection 2 h prior to scanning to map
the relative metabolic activity of tissues within the brain and other soft
tissues of the head. As in the SPECT procedure, the animal was kept in a
quiet, darkened room for 40 min post-injection of the ligand. The dolphin was
then transported as outlined above to the Vital Imaging Facility in Sorrento
Valley, CA, where the PET scan took place. Images were acquired on a Seimens
HR+ PET scanner (Knoxville, TN, USA) with the dolphin on the same specially
engineered bed used in the SPECT scan. A 15-min transmission scan was first
acquired for attenuation correction. The emission scan consisted of eight
frames of 4-min acquisitions to allow for any subject movement. This resulted
in a total scan time of approximately 55 min. The images were converted from
the ECAT 7.2 format to the DICOM 3.0 format for further processing.
Data processing
Data acquired from all of the imaging modalities were processed using
Analyze 4.0/5.0, created by the Biomedical Imaging Resource of the Mayo Clinic
(Robb, 1999;
Robb and Barillot, 1989
;
Robb et al., 1989
). All data
were converted to AVW format (native Analyze format) and volumes made cubic
(equivalent voxel dimensions) through the use of linear interpolation. A
threshold was applied to data from the CT scans according to tissue density
(represented by X-ray attenuation in Houndsfield units), and binary
representations of isolated tissues were created and formed into object maps.
Objects were created for the skull, brain, tympano-periotic complex, surface
of the dolphin and air spaces of the sinus cavities, nasal passages and
larynx. Spatial relationships between structures were observed by visualizing
the objects while suppressing the display of non-objectified tissues. The
volume of air contained in the sinuses and nasal passages was calculated by
multiplying the voxel density of the sinus/nasal passage object by the
calibrated voxel dimensions.
Data from the PET and SPECT scans were co-registered to CT images to localize regions of metabolically active tissues and regions of blood flow. Primary registration was accomplished through application of an automated surface-matching algorithm within Analyze. This algorithm was applied to filled binary objects created from extractions of the brain from both the structural and functional images. Co-registration was achieved by manually fine-tuning the resulting transform matrix after application to the original PET/SPECT and CT image volumes collected from the same animal. PET and SPECT data were also mapped to 24-bit RGB data representations to facilitate visualization of the image volumes.
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Results |
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Utilizing the convention of Fraser and Purves
(1960), the inflated sinus
complex was distinguishable as the primary pterygoid sinus, the mesial and
optic lobes of the pterygoid sinus and a middle ear complex consisting of the
middle, posterior and peribullary sinuses
(Fig. 3). The cranial air space
was compartmentalized by the nasal plugs dorsally and the contracted
palatopharyngeus muscle around the tip of the larynx below. Accessory and
vestibular air sacs were not inflated in WEN, but partial inflation of the
pre-maxillary air sacs was observed in CIN. Air spaces directly abutted the
tympano-periotic complex such that a boneair interface existed
(Fig. 4). Coverage was most
complete on the dorsal, medial and posterior surfaces of the tympano-periotic
complex, with the dorsal surface being almost completely covered by a layer of
air (Fig. 4A,B). Air coverage
of the lateral, ventral and anterior surfaces of the bulla was less complete;
soft tissue connections are known to occur at these sites.
|
SPECT
Uptake of 99mTc-bicisate is indicative of regional blood flow,
and substantial uptake was noted in the brain, melon and posterior region of
the lower jaw, suggesting extensive blood flow within these tissues
(Fig. 5). Uptake by the melon
was greater than four times that of the blubber and surrounding soft tissues
(based upon the number of counts recorded at each site), and the maximum
intensity within the melon was 196% that of the maximum intensity measured in
the brain. (Caution must be exercised when interpreting the difference in
intensity between the melon and brain as resulting from greater blood flow in
the melon than in the brain. 99mTc-bicisate is soluble in lipid and
it is unknown whether the lipid composition of the melon results in a
disproportionate uptake of 99mTc-bicisate relative to the brain for
the same rate of blood flow.) Distribution of ligand in the region of the
melon was greatest in the dorsoanterior portion of the melon, forming an
almost shield-like vascularization that followed the forehead contour
(Fig. 6). The greatest amount
of ligand uptake in the dorsal region of the melon was immediately sub-dermal
while the greatest uptake in the anterior portion of the melon was
approximately 4.5 cm subdermal, posterior to the junction of the forehead and
rostrum. This region presumably contains an increase in connective tissue
proliferation, as has been observed in other odontocete species
(Cranford et al., 1996).
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PET
Three PET scans were taken of subject WEN; however, the field of view (FOV)
was incapable of capturing both the complete melon and brain within the same
scan. The uptake of FDG was demonstratively greater within the brain than in
any other tissue whereas little to no uptake of FDG was observed in portions
of the melon that were within the scan FOV
(Fig. 7). Uptake was observed
in the region of the peribullary, middle and posterior sinuses and appeared to
be consistent with the passage of neural fibers from the brain to the ears
(Fig. 8).
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Discussion |
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It has been proposed that sound refraction can be altered in porpoises by
small variations in the chemical composition of the melon, which subsequently
impact sound speed through the melon
(Varanasi et al., 1975).
Variations in ultrasonic speeds of the inner core (12731376 m
s1) and outer shell (
1682 m s1) of
the melon of the bottlenose dolphin support this notion
(Norris and Harvey, 1974
).
Similarly, temperature-regulated variations in lipid density should affect the
bulk modulus and shear modulus of the melon and fat bodies of the lower jaw as
well as the sound speed through these tissues. Sound speed measured through
the melon of a deceased dolphin was inversely related to temperature of the
melon (Fitzgerald, 1999
), and
although those sound speed measurements are not likely to be equivalent to
measurements recorded in a living animal, the trend will probably be the
same.
Variation in blood flow in response to changing water temperatures may stabilize thermal gradients within the lipid complex of the melon and jaw fats by varying heat availability to these regions. Preservation of thermal gradients within the melon appears particularly feasible given the greater distribution of blood flow over the dorsoanterior portion of the melon, a region that is in close contact with water. A temperature change in the outer shell would alter the sound speed gradient between the outer shell and core of the melon and affect the propagation of echolocation clicks. If no mechanism existed to control the temperature-dependent sound speed gradient of the melon, dolphins experiencing variation in water temperatures would also experience a potentially problematic variation in the collimation of outgoing echolocation clicks. Thus, the ability to stabilize the temperature of the melon would be useful in preserving click propagation characteristics and would be advantageous to dolphin species that inhabit environments with seasonal or regional variations in water temperature.
Ligamentous suspension of the bulla provides for acoustic isolation of the
ears from the skull (Fraser and Purves,
1960; Ketten and Wartzok,
1990
; Reysenbach de Haan,
1956
). Similarly, the presence of air around the bulla contributes
to acoustic isolation of the ears by providing a sound-reflective barrier
between them. The almost complete dorsomedial coverage of the bulla with air
should contribute to the animal's ability to differentiate time of arrival
differences by impeding conduction through soft tissues that exist between the
ears. In combination with other air spaces in the head, this should allow
dolphins to capitalize on spectral differences in received signals due to
shadowing and may contribute to minimum auditory angular resolution in the
vertical and horizontal planes (Popper,
1980
; Purves and Van Utrecht,
1963
; Renaud and Popper,
1975
). Position, geometry and volume of the air spaces within the
head of the dolphin are important components of both the sound production and
reception process and care should be given to their properties when developing
models of biosonar production and hearing in dolphins (e.g.
Aroyan, 2001
).
Anatomical evidence supports the notion that echolocation clicks are
generated by the phonic lips (Cranford et
al., 1996; Evans and Prescott,
1962
) that lie just superior to the nasal plug. The dorsal and
medial air coverage of the bulla, nasal cavity air, the laterally projecting
air-filled pterygoid sinuses, and the skull of the dolphin protect the ear
from the production of echolocation clicks by acting as acoustic reflectors in
the direct path to the ears. However, isolation of the bulla is not complete,
as auditory-evoked potentials are elicited in response to a dolphin's own
echolocation clicks and have been elicited by transmitting synthetic clicks
into the melon of a dolphin (Bullock and
Ridgway, 1972
; Supin et al.,
2003
). For projected clicks, the magnitude of the evoked response
is
20 dB less than that obtained by projecting a click through the lower
jaw, which is commonly believed to be the primary receive channel for echoes
returning from objects ensonified by a dolphin's biosonar pulses
(Brill, 1991
;
McCormick et al., 1970
).
As depth of diving increases, the increasing hydrostatic pressure
diminishes the inspired air volume in accordance with Boyle's Law. Thus, air
within the cranial air spaces will reduce in volume with increasing depth of
diving (Ridgway et al., 1969).
The internal carotid artery of T. truncatus (and other delphinoids)
runs into the middle ear and terminates in the corpus cavernosum carotidis,
which is thought to be an erectile tissue
(Purves, 1966
;
Ridgway, 1968
). Distension of
the corpus cavernosum presumably occurs during diving and reduces the air
volume of the sinus space. Purves and Van Utrecht
(1963
) found that a thin layer
of crystallized salt existed around the ossicles of demineralized specimens of
T. truncatus, even though the corpus cavernosum was apparently
engorged to its fullest extent. It therefore appears that, at full distension,
the corpus cavernosum and peribullar plexus surrounding the middle ear permit
the presence of a thin layer of air. Functionally, this would maintain
acoustic isolation of the ears at depth. Additionally, some amount of air may
be required to permit mechanical motion of ear components (e.g. round window
movement; McCormick et al.,
1970
).
The nasal passages imaged in the dolphins were compartmentalized by closure
of the nasal plug dorsally and constriction of the palatopharyngeus around the
tip of the larynx below. The nasal passages are connected to the air sinuses
of the head via the Eustachian tube. This air is required to drive
the pneumatic click source through pressurization of the nasal cavity
(Ridgway et al., 1980). While
diving, there is an approximate 0.1 MPa increase in pressure for every 10 m
that the dolphin dives, and the volume of air within the sinus and nasal air
space will decline in proportion to increasing air pressure. Volume reductions
in this air space should impact the ability to generate echolocation pulses,
thus requiring a mechanism to replenish the air volume and ensure that a
pressure differential across the phonic lips can be maintained. Under diving
conditions, the palatopharyngeus may mediate exchange between air in the nasal
passages and sinuses and air in the lung
(Ridgway et al., 1980
). Lung
collapse obviates alveolar gas exchange at
70 m depth
(Ridgway and Howard, 1979
),
but movement of air from the lung, bronchi and trachea into the nasal passages
and sinus cavities may compensate for a reduction in air volume within those
anatomical spaces.
Given that a critical volume of air is likely to be required for click and
whistle production and for acoustic isolation of the ears, a theoretical
maximum dive depth at which echolocation pulse generation and hearing
capability are maintained relative to near-surface functionality can be
predicted. Lung volumes between 7 and 11 liters have been estimated for the
bottlenose dolphin (Ridgway et al.,
1969). Assuming a lung volume of 9 liters, and using the
calculated air volume of the sinuses and nasal passages within the dolphin
WEN, a maximum dive depth at which both echolocation and hearing capabilities
are preserved relative to near-surface functionality can be estimated through
the application of Boyle's Law. Further assuming that the nominal amount of
air required to preserve echolocation and hearing functionality is equivalent
to the volume of air measured in the sinuses and nasal passages at the
surface, the maximum depth at which functionality is preserved in the dolphin
WEN is calculated to be
236 m, or 2.5 MPa ofpressure. Depending on the
technique used, the lung volumes of bottlenose dolphins have been estimated to
range from 49 to 71 ml kg1
(Irving et al., 1941
;
Ridgway et al., 1969
) and
probably demonstrate an isometric relationship with mass similar to that
observed in terrestrial mammals
(Schmidt-Nielsen, 1984
;
Kooyman, 1973
). If so, then it
seems reasonable that dolphins with larger masses would have a greater depth
of diving at which echolocation remains possible, providing them with
potential advantages to foraging at depth.
The maximum depth of functional echolocation estimated for WEN is
underestimated if the nasal passages are the only cavities requiring air for
pressurization of the pneumatic click source, i.e. the sinus space may be
diminished to the maximum extent possible through complete distention of the
corpus cavernosum and vascular spaces lining the pterygoid sinuses. A
reduction in the amount of air required for click generation and hearing will
increase the theoretical depth limit at which these functions are preserved.
Similarly, if the total lung volume is underestimated, then the maximum depth
of normal functionality will also be underestimated. Support for a lesser air
volume requirement or greater gas store exists in the observed echolocation of
dolphins to depths of up to 300 m (Ridgway
et al., 1969). Nevertheless, a maximum depth should exist at which
echolocation ceases to be feasible due to a reduction in the volume of gas
inspired prior to descent.
Summary
In the present study, recent anatomical and physiological data from
bottlenose dolphins that were collected with structural and functional
biomedical imaging modalities have provided new insight into the internal
anatomy of the head, relative to the cranial air spaces, and identified
extensive blood flow in relatively metabolically inert fat bodies. Both of
these findings have ramifications to the understanding of dolphin hearing and
echolocation. Air in the sinuses and nasal passages is likely to contribute to
the hearing capability of the dolphin while simultaneously providing the gas
necessary to power the pneumatic source of biosonar pulses. It is speculated
that a reduction in the volume of this air that occurs during descent of a
dive is replenished by the passage of lung air into the nasal passages
via the palatopharyngeus muscle. Blood flow over the melon and within
the posterior regions of the lower jaw is speculated to function as a
thermoregulatory control of lipid density. Thermal regulation of lipid density
within both the melon and jaw fats should maintain sound speed gradients
within these fatty channels, thus preserving the wave guide action of these
sound projection and reception pathways.
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Acknowledgments |
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