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Development and maturation of taste buds of the palatal epithelium of the ratHistological and immunohistochemical study.

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THE ANATOMICAL RECORD 263:260 –268 (2001)
Development and Maturation of Taste
Buds of the Palatal Epithelium of the
Rat: Histological and
Immunohistochemical Study
ASHRAF EL-SHARABY, KATSURA UEDA, KOJIRO KURISU AND
SATOSHI WAKISAKA*
Department of Oral Anatomy and Developmental Biology, Osaka University
Graduate School of Dentistry, Yamadaoka, Suita, Osaka, Japan
ABSTRACT
Palatal taste buds are intriguing partners in the mediation of taste behavior and their
spatial distribution is functionally important for suckling behavior, especially in the neonatal life.
Their prenatal development has not been previously elucidated in the rat, and the onset of their
maturation remains rather controversial. We delineated the development and frequency distribution of the taste buds as well as the immunohistochemical expression of ␣-gustducin, a G
protein closely related to the transduction of taste stimuli, in the nasoincisor papilla (NIP) and
soft palate (SP) from the embryonic day 17 (E17) till the postnatal day 70 (PN70). The main
findings in the present study were the development of a substantial number of taste pores in the
SP of fetal rats (60.3 ⫾ 1.7 out of 122.8 ⫾ 5.5; mean ⫾ SD/animal at E19) and NIP of neonatal
rats (9.8 ⫾ 1.0 out of 44.8 ⫾ 2.2 at PN4). ␣-gustducin-like immunoreactivity (-LI) was not
expressed in the pored taste buds of either prenatal or newborn rats. The earliest expression of
␣-gustducin-LI was demonstrated at PN1 in the SP (1.5 ⫾ 0.5 cells/taste bud; mean ⫾ SD) and
at PN4 in the NIP (1.4 ⫾ 0.5). By age the total counts of pored taste buds continuously increased
and their morphological features became quite discernible. They became pear in shape, characterized by distinct pores, long subporal space, and longitudinally oriented cells. Around the
second week, a remarkable transient decrease in the total number of taste buds was recorded in
the oral epithelium of NIP and SP, which might be correlated with the changes of ingestive
behaviors. The total counts of cells showing ␣-gustducin-LI per taste bud gradually increased till
the end of our investigation (14.1 ⫾ 2.7 in NIP and 12.4 ⫾ 2.5 in SP at PN70). We conclude that
substantial development of taste buds began prenatally in the SP, whereas most developed
entirely postnatal in the NIP. The present study provides evidence that the existence of a taste
pore which is considered an important criterion for the morphological maturation of taste buds is
not enough for the onset of the taste transduction, which necessitates also mature taste cells.
Moreover, the earlier maturation of palatal taste buds compared with the contiguous populations
in the oral cavity evokes an evidence of their significant role in the transmission of gustatory
information, especially in the early life of rat. Anat Rec 263:260 –268, 2001.
©
2001 Wiley-Liss, Inc.
Key words: taste buds; development; ␣-gustducin; nasoincisor papilla; soft palate; rat
Taste transduction is arbitrated by specialized neuroepithelial cells, referred to as gustatory or taste cells that
organize into groups forming taste buds of which the vast
majority are embedded within the lingual and palatal
epithelium. Since Hoffmann (1875) has reported the existence of taste buds on the human palatal mucosa, numerous investigations have been conducted to investigate
their spatial distribution rather than gustatory functions.
The earliest accounts in the rat were published by Kolmer
(1927) and Kaplick (1953) who identified the taste buds in
©
2001 WILEY-LISS, INC.
the nasoincisor papilla (NIP) and soft palate (SP), respectively. Although the palatal taste buds constitute only
*Correspondence to: Satoshi Wakisaka, Department of Oral
Anatomy and Developmental Biology, Osaka University Graduate School of Dentistry, 1-8, Yamadaoka, Suita, Osaka 565-0871,
Japan. E-mail: wakisaka@dent.osaka-u.ac.jp
Received 1 August 2000; Accepted 31 January 2001
Published online 00 Month 2001
DEVELOPMENT AND MATURATION OF PALATAL TASTE BUDS
261
correlation between the onsets of morphological maturation i.e., existence of a taste pore and functional maturation i.e., taste transduction has not previously adopted,
particularly in the developing palate. It is commonly believed that the existence of a distinct taste pore is a unique
morphological criterion for taste bud maturation. Mistretta and Bradley (1977), however, asserted that the existence of elongated, longitudinally-oriented cells should
be additional characteristics of the mature taste buds.
Alpha gustducin has been cloned from taste papillae
isolated from the lingual tissue of rats (McLaughlin et al.,
1992) and microscopic observations suggested that it selectively expressed by cells having the morphological characteristics of matured light cells or type II cells (Tabata et
al., 1995; Yang et al., 2000). Moreover, differential expression of ␣-gustducin were significantly more recognized in
the taste buds highly sensitive to sweet (palatal) or bitter
(foliate and circumvallate) stimuli than fungiform taste
buds that are less sensitive to these compounds (Boughter
et al., 1997). Thus, this protein is thought to be a suitable
marker for matured light cells or type II cells that transduce predominately sweet and bitter stimuli. The present
study was undertaken to trace the detailed temporal and
spatial distribution of taste buds in the NIP and SP, which
may be correlated with the critical changes in ingestive
behavior during development. The demonstration of
␣-gustducin in the developing palatal taste buds was also
designated to investigate the onset of their functional
maturation i.e., taste transduction and its correlation with
the morphological maturation and the existence of taste
pores.
MATERIALS AND METHODS
All experiments were reviewed and approved by Osaka
University Graduate School of Dentistry Intramural Use
and Care Committee before the study.
Animals and Tissue Preparation
Fig. 1. A: Transverse view of the nasoincisor papilla. The epithelium
of the nasoincisor papilla is divided into two regions; nasoincisor ductural epithelium (NID) and oral epithelium (OE), which is further subdivided into epithelium of the papillary dome (DE) and epithelium lateral to
the NID (LE). C, cartilage. B: Surface view of the palate. Soft palate (SP)
is also divided into two regions; Geschmacksstreifen (GS), the border
between SP and hard palate (HP), and posterior palatine field (PPF). T,
molar teeth; TR, terminal ridge; NP, nasopharyngeal orifice.
17% of the entire oropharyngeal complement in the adult
rat (Miller, 1977), their approximate topography to their
fellows in the fungiform, circumvallate and foliate papillae as well as epiglottal surface revealed a curious identity
(Miller and Spangler, 1982). Moreover, their spatial distribution is functionally important for the suckling behavior in pre-weanling animals as milk stimulates them
much more than the lingual taste buds (Ardran et al.,
1958). In the neonatal rat, Harada et al. (2000) assigned
that the number of pores in the SP of the rat at birth is
significantly higher than the lingual taste bud populations, which reflects the crucial contribution of palatal
taste buds in the mediation of taste directly after birth. In
contrast to the contiguous taste bud populations, whether
those of the palate begin their development prenatally or
postnatally has not previously elucidated. Moreover, the
Forty-four Sprague–Dawley rats of both genders were
used for statistical analysis by ordinary hematoxylineosin (HE) staining in addition to 33 rats for the immunohistochemical investigation for ␣-gustducin. All animals were purchased from Nihon Dobutsu, Osaka, Japan.
The day on which a vaginal plug was confirmed was designated as “embryonic day (E) 0.” Pregnant animals at
various stages were sacrificed by overdose i.p. injection of
chloral hydrate (600 mg/kg) and the fetuses were collected. The whole palates were dissected out and immersed in 4% paraformaldehyde in 0.1 M phosphate
buffer (pH 7.4) for 3 days. For postnatal development, the
day of birth was designated as “postnatal day (PN) 0.” The
animals at various postnatal days were deeply anesthetized with i.p. injection of chloral hydrate (600 mg/kg) and
perfused transcardially with 0.02 M phosphate-buffered
saline (PBS; pH 7.2) followed by 4% paraformaldehyde.
The heads were removed and placed in the same fixative
for 3– 4 days. Specimens from rats at PN15 and older were
decalcified with 7.5% ethylene diamine tetraacetic acid
(EDTA) for 1– 6 weeks at 4°C with continuous shaking and
weekly change. The palates were removed from the transverse terminal ridge caudally to the nasopharyngeal orifice, whereas the central part rostral to the first antemolar
ruga containing nasoincisor ducts was excised. All specimens were dehydrated by an ascending series of ethanol,
262
EL-SHARABY ET AL.
Fig. 2. Photomicrographs of the developing palatal taste buds. A: A
nonpored taste bud is recognized in the SP at E19. B,C: Pored-taste
buds are detected in the SP at E19 (B) and in the NIP at PN4 (C). Cells
in these pored taste buds sparsely arranged. Arrows indicate the taste
pores. D: Pored-taste bud in the SP at PN7. Cells within the taste buds
showed typical pear-shaped characteristics. EP, epithelium; LP, lamina
propria. Scale bar ⫽ 30 ␮m.
cleared in xylene and embedded in paraffin. The nasoincisor ducts were oriented for sectioning in the transverse
plane, whereas the SPs were oriented to cut parasagittally. Complete serial sections cut at 6 –10 ␮m thickness,
were mounted on glass slides and stained with routine HE
staining for the statistical analysis.
For the immunohistochemistry, serial sections were cut
at a thickness of 8 –10 ␮m and mounted on ploy-L-lysinesubbed glass slides. They were deparaffinized in xylene
and rehydrated through descending series of ethanol. The
sections were treated in 0.1 M sodium citrate buffer (pH
6.0) for 10 min in a microwave for antigen retrieval (Cattorretti et al., 1992). Avidin-biotin-complex (ABC) method
was applied for demonstration of ␣-gustducin-like immunoreactivity (-LI). The sections were treated with absolute
methanol containing 0.3% H2O2 for 30 min to block endogenous peroxidase activity. They were then incubated
overnight at room temperature with ␣-gustducin antiserum (1:1,000; Santa Cruz Biotechnology Inc., Santa
Cruz, CA). After PBS rinse, the sections were incubated
with biotinylated swine anti-rabbit IgG (1:500; Dako,
Copenhagen, Denmark), followed by PBS rinse and subsequently with ABC complex (Vector, Burlingame, CA) for
90 min each at room temperature. Horseradish peroxidase
activity was detected by incubating the slides with 0.1 M
Tris-HCl buffer (pH 7.5) containing 0.04% 3-3⬘ diaminobenzidine trihydrochloride (DAB) and 0.003% H2O2. The
DAB reactions were enhanced by 0.08 – 0.1% nickel ammonium sulfate. The immunostained sections were counterstained with methyl green, dehydrated with a graded
series of ethanol, cleared in xylene, coverslipped with Permount (Fisher Scientific Inc., Fairlawn, NJ) and examined
by light microscope.
Photographic images were captured on CCD camera
mounted on an Olympus microscope. Images were prepared for printing with Photoshop (Ver. 5.0, Adobe Systems, Inc., San Jose, CA), and printed out by a Fujix
Pictrography 3000 digital photographic printer (Fuji
Photo Film). Contrast was adjusted as needed.
The specificity of the primary antibody was checked by
preabsorption test. The sections were incubated with preabsorbed primary antibody with excess amount of antigen
(10 ␮g/ml of diluted primary antibody; Santa Cruz Bio-
technology Inc.), resulting in no immunoreactions. For
control of immunohistochemical procedure, the primary
antibody was replaced with nonimmune serum or PBS. In
addition, the incubation with secondary antibody or the
ABC complex was also omitted. These sections had no
immunoreactions.
Quantification of the Data
We traced the spatial distribution of taste buds in the
palate of rats during the prenatal development (E17–20;
daily intervals) and at various postnatal ages (PN1, 4, 7,
15, 21, 35 and 70; n ⫽ 4 for each age). Each of the NIP and
SP was divided into two areas (Fig. 1A,B). The epithelium
of NIP was divided into ductal epithelium (right and left
nasoincisor ducts) and oral epithelium (dome of the papilla and adjacent oral epithelium lateral to the two nasoincisor ducts). The SP was divided into a transverse fold,
directly posterior to the terminal ridge of hard palate,
referred to as Geschmacksstreifen (GS) and a perpendicular central zone referred to as posterior palatine field
(PPF). The existence of a taste pore was used as a criterion
to distinguish the morphological stage i.e., nonpored and
pored taste buds of the palate. For numerical analysis of
the taste buds in each region of the palate, every profile of
a taste bud, with or without a taste pore in each serial
section of the NIP and SP was counted. In the SP, we
delineated the zone where the taste buds were distributed
at each stage and measuring the distance between the bud
and GS or posterior border of the PPF. All taste buds were
serially reconstructed on schematic drawings of the palatal structures to ensure that each bud was counted only
once. The numbers of all taste buds in the NIP and SP
were counted and graphically represented.
The immunohistochemical demonstration of ␣-gustducin was used to recognize the onset of functional maturation i.e., taste transduction of the palatal taste buds and
its relation with their morphological features or existence
of a taste pore. Prenatal ages (E18 –20; daily intervals)
and postnatal ages (PN1, 2, 4, 7, 15, 21, 35 and 70; n ⫽ 3
for each age) were used. In each of the NIP and SP, 20
taste buds were randomly selected per animal to count
␣-gustducin-immunoreactive (-IR) cells. Every cell profile
containing a nucleus was counted once. The total counts of
DEVELOPMENT AND MATURATION OF PALATAL TASTE BUDS
263
Fig. 3. Temporal changes in the number of taste buds at the nasoincisor papilla of the developing rat. Top panel shows the total number
of taste buds, and middle and lower panels indicate the number of taste
buds in the nasoincisor duct and oral epithelium, respectively.
␣-gustducin-IR cells per taste bud in the NIP and SP were
recorded at different ages.
RESULTS
Morphology of the Developing Palatal Taste
Buds
The nonpored taste buds were first recognized as spherical masses of columnar cells extended from the basal
lamina to a variable distance toward the surface epithelium of the SP and NIP at E18 and E20, respectively (Fig.
2A). These buds acquired a more elongated shape and
short neck such that they access the oral cavity via a
narrow taste pore (4 – 6 ␮m in diameter) at E19 and PN4,
in the SP and NIP, respectively. At these early stages of
development, the cells in the pored taste buds were almost
sparsely arranged with ovoid nuclei and somewhat eosinophilic cytoplasm and not reached the taste pore (Fig.
2B,C). Toward the end of the first week, the morphological
features of pored taste buds became quite discernible.
They became pear in shape and characterized by a distinct
pore, long subporal space and longitudinally oriented cells
pointed toward the pore (Fig. 2D).
Fig. 4. Topographic localization of taste buds at the nasoincisor
papilla of the rat at E20 (A) and PN 70 (B). One open dot represents one
nonpored taste bud, while one closed dot represents one pored taste
bud. C, cartilage.
Temporo-Spatial Distribution of Taste Buds in
the NIP During Development
The length of NIP measured about 300 – 450 ␮m at E20
and reached 1.3–1.7 mm at PN70. The orifices of right and
left nasoincisor ducts occupied the third quarter of the
papilla and measured 120 ␮m at E20 and 500 ␮m at
PN70. Figure 3 and 4 show the temporal and spatial
distribution of taste buds along the NIP. At E20, 8.5 ⫾ 1.0
taste buds (mean ⫾ SD/animal) were the earliest account
along the oral epithelium of the posterior half of the NIP,
and all of them belonged to the immature type (nonpored
taste buds). They were distributed in the dome region as
well as lateral folds of the papilla; medial and lateral to
264
EL-SHARABY ET AL.
the orifices of nasoincisor ducts (Fig. 4A). At PN1, 11.0 ⫾
2.0 buds appeared in the medial aspect of the nasoincisor
ducts. Along the first few days, a gradual proliferation was
recorded over the whole papilla and the number of nonpored taste buds in the oral epithelium was still higher
compared with the nasoincisor ducts i.e., 17.8 ⫾ 3.3 and
16.3 ⫾ 2.1 at PN4, respectively. The earliest existence of
taste pores was found simultaneously but higher in the
oral epithelium (4.8 ⫾ 0.5) than ductal epithelium populations (3.8 ⫾ 1.0). At PN15, the count of pored taste buds
within the nasoincisor ducts exceeded that of the contagious parts of oral epithelium (40.3 ⫾ 8.8 and 19.3 ⫾ 4.6,
respectively). A transient decrease in the total number of
taste buds was demonstrated in the oral epithelium
around the second week. At the end of our investigation,
the total count of the taste buds within the nasoincisor
ducts was approximately twice that in the oral epithelium
i.e., 61.8 ⫾ 1.9 and 27.8 ⫾ 2.5, respectively (Fig. 4B). No
significant differences were recorded in the taste bud populations within the right and left nasoincisor ducts.
Temporo-Spatial Distribution of Taste Buds in
the SP During Development
In all investigated specimens, the taste buds were
uniquely distributed along T-shaped zone whose transverse part, an incomplete fold known as Geschmacksstreifen (GS), whereas the perpendicular part extended to the
nasopharynx known as posterior palatine field (PPF). In
the GS whose length was 1.6 –5.6 mm, the taste buds were
constantly and densely distributed on both sides of a central zone ranged between 120 –250 ␮m at E18 and PN70,
respectively. On the other hand, the buds were variably
distributed within a central zone of the PPF whose width
were approximately 0.7 and 2.5 mm at E18 and PN70,
respectively. Figure 5 and 6 show the temporal and spatial
distribution of taste buds along the SP. Proliferation of
nonpored taste buds occurred mostly before birth, however, a comparable number was also developed along the
first 3 weeks after birth. A total of 16.5 ⫾ 3.1 taste buds in
the GS as well as 37.5 ⫾ 6.8 along the middle half of PPF
were first recognized at E18 (Fig. 6A). The earliest recognition of taste pores was recorded simultaneously in GS
and PPF at E19 (21.0 ⫾ 2.6 and 39.3 ⫾ 2.2, respectively).
Although the taste pores concentrated peripherally in GS,
they were concentrated more posteriorly in the PPF. At
PN1, the number of the taste buds with pores reached
52.0 ⫾ 3.4 and 64.3 ⫾ 3.2 in the GS and PPF, respectively.
A gradual increase in the number of pores was traced
along the first week with a higher incidence in the GS. At
the second week, a transient decrease was recorded in the
number of pored buds in both GS and PPF (Fig. 5). Toward
the end of our investigation, the majority of taste buds
were traced along the posterior 3⁄4 of PPF compared with
its anterior 1⁄4 and 266.3 ⫾ 16.5 pored taste buds were
recorded on the whole palate, with a double incidence in
the PPF compared with GS (Fig. 6B).
Immunoreactivity of ␣-Gustducin in the
Developing Palatal Taste Buds
Figure 7 traces the counts of ␣-gustducin-IR cells per
taste bud at different stages of development on both the
NIP and SP. The immunoreactivity for ␣-gustducin could
not be identified in the nonpored taste buds, which continued proliferation on the palatal epithelium for the first
Fig. 5. Temporal changes in the number of taste buds at the soft
palate of the developing rat. A: Indicates total number of taste buds.
B,C: Indicates the number of taste buds in the Geschmacksstreifen and
posterior palatine field, respectively.
3 weeks after birth (Fig. 8A). Moreover, no immunoreactivity could be detected among the pored taste buds developed prenatally or shortly after birth in either the SP or
NIP (Fig. 8B). At PN1, ␣-gustducin-LI was recognized in
some pored taste buds of the SP (1.5 ⫾ 0.5; mean ⫾ SD),
whereas others lacked such immunoreactivity (Fig. 8C).
Meanwhile, ␣-gustducin-IR taste cells (1.4 ⫾ 0.5) could be
recorded in the NIP at PN4 (Fig. 8D). Occasional taste
buds containing only one gustducin-IR cell, however, were
recognized in the oral epithelium of the papilla in some
PN2 rats. Cells immunoreactive for ␣-gustducin were
spindled-shaped, longitudinally-oriented having ovoid nuclei and a smooth regular outline throughout their length
with a larger diameter at the nuclear region tapering to a
smaller diameter at either ends. A pronounced immunoreactivity was evenly distributed throughout the cytoplasm from the apex where apical processes converged at
the taste pore to the basal region of the taste bud. By age,
a gradual increase in the counts of ␣-gustducin-IR cells
was recognized in the taste buds of the developing NIP
and SP (Fig. 8E,F). Significantly higher counts were re-
DEVELOPMENT AND MATURATION OF PALATAL TASTE BUDS
265
Fig. 7. Temporal changes in the number of ␣-gustducin-immunoreactive (-IR) cells per taste bud in the nasoincisor papilla (E) and the soft
palate (F) of the developing rat.
Fig. 6. Topographic localization of taste buds at the soft palate of the
rat at E18 (A) and PN70 (B). One open dot represents one nonpored taste
bud, and one closed dot represents one pored taste bud. Taste buds are
concentrated at the Geschmacksstreifen (GS) and middle portion of the
posterior palatine field, forming T-shaped distribution.
corded in the NIP as compared with the SP at the third
week and older ages. At PN70, 14.4 ⫾ 2.7 and 12.4 ⫾ 2.5
cells were immunoreactive for ␣-gustducin in single taste
bud in the NIP and SP, respectively.
DISCUSSION
Temporal and Spatial Development of the
Palatal Taste Buds
The prenatal development of the palatal taste buds was
traced in mammalian species such as humans, monkeys,
sheep, and cats as well as hamsters (Bradley and Stern,
1967; Bradley et al., 1979; Stedman et al., 1983; Zahm and
Munger, 1983; Belecky and Smith, 1990). The present
study revealed that the development of rat taste buds is
almost prenatal in the SP, whereas most entirely postnatal in the NIP. Proliferation of the nonpored taste buds in
the whole palatal epithelium was recognized along the
first 3 weeks after birth, whereas the counts of pored taste
buds continuously increased till the end of our investigation. In the SP, the earliest account of nonpored taste buds
was traced at E18, whereas the pored ones developed at
E19. A substantial number of pored and nonpored buds
were demonstrated at E20 (i.e., about 60% of those recorded in adult; PN70). Harada et al. (2000) reported that
53% of the taste buds in the SP contained a taste pore at
birth, which is consistent with the present study. Our
findings, however, contrast with Mistretta (1972) who recognized taste buds in the neonatal rats but concluded that
they should be morphologically immature at birth. Srivastava and Vyas (1979) reported that they were absent in
newborn rats, developed along the first 3 weeks of age, and
after this stage there is no taste bud formation. Regarding
the taste buds in the NIP, the nonpored buds were recognized at E20 whereas the pored ones developed at PN4.
Settembrini (1987) recorded taste bud primordia in the
newborn rats but confirmed that these should be regarded
as morphologically mature by the second week of postnatal life. Harada et al. (2000) recorded five to seven taste
buds within the nasoincisor ducts at birth; one of which
contained a taste pore. In the NIP of the mouse, OhtaYamakita et al. (1982) stated that the taste buds appear at
4 or 5 days, matured at 10 days of age and there is a
continuous taste bud formation in the papilla over the first
10 weeks of age. Taken together with this evidence, it is
concluded that the morphological maturation of the taste
buds, i.e., presence of the taste pores, occurs in the SP
prenatally and in the NIP at early days after the birth.
The present study revealed that the taste buds were
scattered between two populations in the NIP, ductal epithelium (medial aspect of the distal part of nasoincisor
ducts), and oral epithelium (oral surface of the dome and
the epithelium lateral to the papilla). The taste buds in
the SP were uniformly distributed within a T-shaped zone
266
EL-SHARABY ET AL.
Fig. 8. Photomicrographs of ␣-gustducin-like immunoreactivity in
the nonpored (A) and pored taste buds (B–F) of the epithelium of soft
palate (A–C,E) and nasoincisor papilla (D,F) of the developing rat. A: No
immunoreactivity is detected in the nonpored taste bud in the soft palate
at E20. B: A pored taste bud in the soft palate at PN1 has no immunoreactivity. An arrowhead indicates the taste pore. C,D: A pored taste bud
has two or three ␣-gustducin-immunoreactive (-IR) cells in the soft
palate at PN1 (C) and in the nasoincisor papilla at PN4 (D). E,F: At PN70,
taste buds in the soft palate (E) and nasoincisor papilla (F) contain five or
more ␣-gustducin-IR cells. Scale bar ⫽ 10 ␮m (A,B,D,E); scale bar ⫽ 50
␮m (F).
composed transversely from the incomplete GS fold and
perpendicularly from the PPF at all stages of development. These findings are almost in agreement with the
previous investigations (Miller and Spangler, 1982; Ohta-
Yamakita et al., 1982; Miller and Smith, 1984; Settembrini, 1987; Harada et al., 1997a), but the detailed topographic distribution of taste buds in the SP, as shown in
Figure 6 is different from that reported by Harada et al.
DEVELOPMENT AND MATURATION OF PALATAL TASTE BUDS
(1997a). We think such difference is due to the variation
among the individual animals, as Miller and Spangler
(1982) reported the different topographic distribution pattern among the individual animals. Although the topographic distribution pattern of the taste buds in the SP
has been reported, the existence of appreciable number of
taste buds along the oral epithelium of NIP has not previously taken into detailed consideration. Simultaneous
deposition of the taste buds and subsequently their pores
were recorded prenatally in the GS and PPF of the SP.
Their development was traced most entirely after birth in
the NIP where it was earlier in the oral epithelium than
the nasoincisor ducts. Such particular deposition indicates
the functional role of taste bud populations in the SP and
oral epithelium of the NIP compared with that of the
nasoincisor ducts along the first week of life. Around the
second week, the count of pored buds within the nasoincisor ducts began to exceed that of the contiguous parts of
the papilla, whereas a transient decrease was evidently
recorded not only in the oral epithelium of NIP but also
over the whole SP.
Taste Transduction and Morphological
Maturation of the Palatal Taste Buds
Taste transduction is initiated at the taste pore of a
taste bud where microvilli of the mature taste cells make
contact with the outside environment. In the present
study, the existence of a substantial number of distinct
pores in the palate of fetal and newborn rats aroused
interesting inquiries about the relationship between taste
input and behaviors that depend upon this sensory system. Hall and Bryan (1981) stated that rats as young as
1–3 days of age shows differential responses to oral infusion of sucrose vs. water, which undoubtedly elucidates
that functional taste buds should be present to mediate
these ingestive responses. Contribution of the palatal
taste buds to the taste mechanism in the neonatal rats
became conceivably more crucial because Harada et al.
(2000) ascertained that 53% of the taste buds in the SP
contained a taste pore at birth compared with only 14%
within fungiform papillae; whereas no pores were observed within foliate and circumvallate papillae. In the
present study, the onset of taste transduction triggered by
the earliest ␣-gustducin-IR cells recognized at PN2 (1.6 ⫾
0.5) and PN4 (1.4 ⫾ 0.5) in the SP and NIP, respectively.
Because the morphological observations suggested that
␣-gustducin is selectively expressed by mature taste cells;
light or type II cells (Tabata et al., 1995; Yang et al., 2000),
these cells should be absent in the all palatal taste buds of
fetal and some of the neonatal rats or apparently still
immature. Mistretta and Bradley (1977) asserted that the
existence of elongated, longitudinally-oriented cells
should be additional characteristics of mature taste buds.
Moreover, ultrastructural and electrophysiological observations hypothesized the existence of transitional elongated cell type i.e., developing taste cells that had not
reached the taste pore (Mackay-Sim et al., 1996). Interpreting with these studies, the present findings disclosed
that the taste pore might be no longer a substantive criterion for the maturation of taste buds as it is still commonly believed. Instead, the existence of the pore cooperated by the mature taste cells is essential for the onset of
taste transduction. The absence of these cells in the palate
of neonatal rats may indicate that feeding stimulation
267
such as suckling is an essential signal for taste transduction.
Function of the Palatal Taste Buds During
Development
Electrophysiological observations on the gustatory stimuli of the peripheral taste fibers argued that the greater
superficial petrosal nerve, which innervates the palatal
taste buds, is most responsive to sweet-tasting stimuli
(Nejad, 1986; Harada et al., 1997b). In support, ␣-gustducin, which is strongly implicated in the mediation of
sweet-tasting substances, was strongly expressed in the
palatal taste buds (Boughter et al., 1997). The present
findings and interpretations on the previous investigations (Miller and Spangler, 1982; Harada et al., 2000)
aroused great evidence about the gustatory functions of
the palatal taste buds in the neonatal life and their temporal collaboration with contiguous taste bud populations.
It is important to emphasize that the onset of sweet transduction in the rat began by the PN1 on the SP and PN4 on
the NIP. During the first few days, it is conceivable that
the discernible number of soft palatal taste buds collaborated anteriorly by fungiform taste buds accomplish the
overall taste behavior, whereas the nasopalatal buds can
efficiently share in the taste responses by the end of the
first week. Around the second week, a transient decrease
in the total counts of taste buds with a relatively insufficient number of ␣-gustducin-IR cells/taste buds may be
attributed to the progressive changes in the suckling and
behavioral responses to varied food intake (Blass et al.,
1979). This might be maintained by the developing foliate
and circumvallate taste buds, which achieved a significant
maturity around this age (Harada et al., 2000). We conclude that a substantial development of taste buds began
prenatally in the SP, whereas most entirely postnatal in
the NIP and the existence of both the taste pore and
mature taste cells is essential for taste transduction.
Moreover, the earlier maturation of palatal taste buds
compared with the contiguous populations in the oral cavity raises evidence of their significant role in the taste
mechanism, especially in the early life of the rat.
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development, taste, epithelium, immunohistochemical, palatal, buds, stud, maturation, rathistological
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