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Long-term effects of gustatory neurectomy on fungiform papillae in the young rat.

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THE ANATOMICAL RECORD 225:224-231 (1989)
Long-Term Effects of Gustatory Neurectomy on
Fungiform Papillae in the Young Rat
JUDITH R. GANCHROW AND DONALD GANCHROW
Department of Oral Biology, The Hebrew Uniuersity-HadassahFaculty of Dental Medicine
Founded by The Alpha Omega Fraternity, Jerusalem 91 -010 (J.R.G.),and Department of
Anatomy and Anthropology, Sackler Faculty of Medicine, Tel-Aviv University, Ramat Aviv
69-978, Tel - Aviv (D.G .),Israel
ABSTRACT
Recent evidence from mature hamster fungiform papillae indicates that following denervation taste buds are present from 21 to 330 days in the
absence of discernible intragemmal nerve fibers. In contrast, most prior taste bud
degeneration studies focused on shorter survival times. The present inquiry in
young rats examined the issue of postneurectomy buds, in which regeneration of
the resected chorda tympani or facial nerves was prevented and anterior tongue
tissue examined over a range of relatively long survival times (30-90 days). Conditions for observing potential taste buds used three histologic stains and a definition of the taste bud not necessarily requiring pore identification.
In each case, serial section examination of the anterior-most 2-3 mm of lingual
epithelium revealed 29-56 bud-containing fungiform papillae on the unoperated
side. In contrast, ipsilateral to the neurectomy, only zero-7 medially-placed,
mature-looking buds were observed per case, as well as zero-3 more laterally
situated fungiform papillae containing small clusters of cells in basal epithelium
that lacked the vertical organization and cytoplasmic staining intensity of mature
taste buds. These cell aggregates were distributed evenly across survival time and
stain used.
Therefore, in young rats following gustatory neurectomy, longer survival times,
per se, would not appear to be a prerequisite for sustaining fungiform taste buds.
The appearance of “midline” buds postsurgery may be attributed to either normal
contralateral or a net bilateral innervation, andlor ipsilateral denervation and bud
loss inducing neural sprouting from the contralateral side.
For more than a century it has been maintained that
taste bud survival is critically nerve-dependent (e.g.,
von Vintschgau and Honigschmied, 1877; also see Table 1). It is typically reported that damage to a gustatory nerve results in degeneration and disappearance
of taste buds in the relevant oral sensory epithelium
and should appropriate reinnervation of the taste target tissue occur, the buds, in turn, regenerate. Only
gustatory or arterial chemosensory neurons seem capable of supporting taste bud regeneration in the oral
cavity, and not cutaneous sensory or motor neurons
(e.g., Dinger et al., 1984; Guth, 1958; Oakley, 1974;
State, 1977; State et al., 1982; Zalewski, 1969b, 1970).
Recently, the concept of taste bud neural dependence
has been challenged. Whitehead et al. (1987) reported
that taste buds in fungiform papillae of adult hamsters
persisted for as long as 330 days following chorda tympani resection. Care was taken to prevent neural regeneration to the denervated area, and electron microscopic analysis failed to reveal any neuron profiles in
the budlike configurations observed. Both dark and
light cells could be visualized in buds on the operated
and unoperated sides. In addition, buds on the operated
side seemed smaller and had no easily stainable taste
pore communication with the oral cavity (see also Hou
et al., 1985).
0 1989 ALAN
R. LISS. INC
In contrast, for example, the present authors reported that chicken taste buds are completely absent
11-21 days following chorda tympani resection (Ganchrow et al., 1986).Epithelial organization in the denervated tissue was devoid of incipient, developing, or mature taste buds during the postoperative period studied
by serial section analysis. However, oral taste buds in
chickens are not contained within specialized papillae
(e.g., Berkhoudt, 1985; Ganchrow and Ganchrow, 1987;
Gentle, 1971; Gentle and Hunter, 1983; Saito, 1966)
that, conceivably, could provide some maintenance
function for degenerating or newly forming taste buds.
Furthermore, on the operated side, Whitehead et al.
(1987) saw buds in an apparently degenerative phase
at 8 days, but did not examine materials in the 9-20
postoperative-day interval. Perhaps taste buds do completely disappear in this later interval, as is accordingly recorded by various authors, and then show limited regeneration over more extended periods of time.
Received March 10, 1988; accepted January 5, 1989.
Address reprint requests t o Dr. Judith R. Ganchrow, The Hebrew
University-Hadassah Faculty of Dental Medicine, P.O. Box 1172,
Jerusalem 91-010, Israel.
225
CHORDA TYMPANI NEURECTOMY
TABLE 1. Results of gustatory nerve damage in vertebrates as related to age,’ target tissue, survival time, and
staining technique
Species
Rat2
Rat2
Rat
Rat3
Rat4
Rat4
Rat4
Rat2
Nerve
Survival
damaged time (days)
7
VII
24-25
VII
VII
7
IX
7-87
7-10
IX
IX
7
IX
35
1-5
IX
Rat2
IX
IX
IX
Rat
Rat
IX
IX
Rat
IX + VII
Rat4
Gerbi12,4
VII
VII
Gerbil2
VII
Hamster2
Hamster
VII
IX
Rabbit4
Rat2
Rabbit2
Rabbit’
Rabbit
Rabbit
Rabbit
Cat
Cat‘
Monkey’
Monkey2
Chicken3
Chicken4
Duck
Frog
Catfish2
Catfish
Catfish
Catfish
Catfish
IX
IX
IX
IX
IX
VII
VII
IX
VII
VII
IX
VII
IX
VII
IX
VII
IX
VII
VII
VII
VII
VII
Tissue
examined
FP
FP
FP
CP
FOP
CP
CP
CP
7-2 1
14-100
21
21
10-30
14-140
7-9
15
1-8
21-330
82-143
FOP
CP
CP
CP
CP
FOP
FP
FP
FP
FP
CP and FOP
6-10
21-120
10-21
17-35
14-18
8-15
13
28
16-19
24-27
42-140
8
21-30
11-21
10-46
7-10
42-300
15-37
18-33
14-17
12
10-15
CP and FOP
CP and FOP
CP
FOP
FOP
FP
FP
CP
FP
FP
CP
FP
CP
ALB
Bud cells
remain (x)
X
X
X
X
X
X
-
PT
-
P
FP
B
B
B
B
B
X
X
X
-
-
Stain
EM (electron microscopy)
Iron hematoxylin
Not listed
Iron hematoxylin
EM
Iron hematoxylin
Iron hematoxylin
Picro-fuchsin;
Weigert hematoxylin
Immunostaining, substance P
Enzyme reactions
Iron hematoxylin
Iron hematoxylin
Enzyme reactions
Methyl green; enzyme reactions
Iron hematoxylin; silver
Iron hematoxylin
EM
EM
Osmic acid
Hematoxylin & eosin (H & E)
H&E
EM
EM
EM; paraphenylendiamin
Phosphotungstic hematoxylin
Phosphotungstic hematoxylin
Enzyme reactions
Delafield‘s hematoxylin
Methylene blue
Iron hematoxylin; protargol
EM
H & E; silver
H&E
H&E
Silver
Iron hematoxylin
Silver
Silver
Iron hematoxvlin
Iron hematoxylin; H & E
Iron hematoxylin; H & E
Author(s)
Farbman, 1969
Whiteside, 1927
Beidler, 1963
Hosley et al., 1987
Chelyshev et al., 1982
Guth, 1957
Guth, 1963
Kennedy, 1972
Nishimoto et al., 1985
Zalewski, 1981
Oakley, 1970
Oakley, 1974
Zalewski, 1970
Zalewski, 1969a
Cheal and Oakley, 1977
Sloan et al., 1983
Whitehead et al., 1985
Whitehead et al., 1987
von Vintschgau and
Honigschmied, 1877
State and Dessouky, 1977
Naga et al., 1970
Fujimoto and Murray, 1970
Iwayama, 1970
Jeppsson, 1969
Olmsted, 1921
Olmsted, 1922
State et al., 1982
Hayes and Elliott, 1942
Langworthy, 1924
Guth, 1958
Zahm and Munger, 1985
Vij et al., 1972
Ganchrow et al., 1986
Gentle, 1971
Krol and Dubbeldam, 1979
Robbins, 1967
Kamrin and Singer, 1953
May, 1925
Olmsted. 1920
Torrey, 1934
Torrey, 1936
Abbreviations: ALB-anterior lower beak oral epithelium; B-barbels; CP-circumvallate papillae; FP-fungiform papillae; FOP-foliate
apillae; P-palate; PT-posterior tongue.
‘Age, puberty, breeding, and weight relationships were obtained from Holmes (1984),Koch (1973),and Weisbroth (1984)if not specifically
indicated in the study referenced.
2Adults (at surgery).
3Prepubertal.
4Peripubertal.
Table 1 summarizes some previous studies on budnerve dependency in order to ascertain which factors
may have been critically linked to the conclusions
drawn. An “x” in the column titled “Bud cells remain”
indicates that complete buds, or some fusiform cells or
other budlike structures, could be discerned in the epithelial position where one would expect to find a bud.
The symbol “-” indicates no buds were discovered after
gustatory nerve damage. Footnotes 2,3, and 4 indicate
maturity of each species for studies that mention that
variable. As can be seen from this table, there is no
obvious relation between reported surviving “buds”
and species, age, stain, o r taste bud locus.
Of the 41 studies presented, 54% claimed the taste
buds totally disappeared, and 82% of these latter reports based their results on tissue examined in the
postoperative interval between 1 and 5 weeks. An additional 29% reported total bud disappearance with the
exception of a few buds o r budlike figures still remaining. Likewise, most (75%)of these latter studies examined the 1-5 week postoperative interval. Some authors account for the scant buds remaining during the
degenerative period either as midline-region buds receiving contralateral innervation (e.g., Cheal and Oakley, 1977; Hayes and Elliott, 1942; Guth, 1958; State et
al., 1982; Whiteside, 1927) or by the incompleteness of
J.R. GANCHROW AND D. GANCHROW
226
Wallerian degeneration in the sectioned nerve (e.g.,
Kamrin and Singer, 1953) or by the coincidental occurrence of regeneration when nerve regrowth could not
be ruled out (e.g., Hosley et al., 1987). In addition, of
ten studies reporting presence of buds or bud cells
(Cheal and Oakley, 1977; Chelyshev et al., 1982; Farbman, 1969; Fujimoto and Murray, 1970; Kennedy,
1972; Krol and Dubbeldam, 1979; Olmsted, 1921,1922;
Sloan et al., 1983; Whitehead et al., 1985), nine examined tissue between 1and 15 postoperative days, which
may be early for complete degeneration to have occurred, under their experimental conditions. In one instance of longer survival, von Vintschgau and Honigschmied (1877) reported that the place where the buds
had been located was noticeable, suggesting some kind
of nonstratified epithelial cell organization lacking
typical bud features. In the rabbit (Jeppsson, 19691, rat
(Zalewski, 1969a; 1981), and chicken (Gentle, 1971) after survival times of up to 6 months, 3-5 months, and
6 weeks, respectively, glossopharyngeal-innervated
taste buds unequivocally disappeared: “The permanent
loss of buds in chronically denervated papillae verifies
that buds do not regenerate spontaneously in the absence of appropriate innervation” (Zalewski, 1981, p.
310). However, the latter author used cholinesterase
and ATPase stains to mark the reactions, and conceivably, potentially remaining buds could have physiological characteristics refractory to these stains.
In summary, most studies reporting total bud disappearance in fungiform papillae used survival times up
to 27 days. Following glossopharyngeal neurectomy,
total bud loss occasionally has been sustained beyond
100 days, but, in general, mammalian examples using
a postneurectomy time frame beyond 1 month are noticeably lacking. The present study in the young rat
extended the survival time period to include 30-90 days
postneurectomy to see whether bud presence could be
identified within this relatively longer postoperative
interval. Also, the majority of previous reports (Table 1)
used hematoxylin stains. The present study incorporated this stain plus two others so as to decrease the
possibility that postneurectomy buds in these young
animals would be refractory to a single epithelial stain
and escape identification. Surgery was performed in the
fifth postnatal week, after weaning was complete. This
relatively young prepubertal age may highlight a critical taste bud-neural dependency or, conversely, optimize the potential for plasticity and regenerative capacity since gustatory system maturation progresses
gradually over the first 90 postnatal days in rats (e.g.,
Farbman, 1965; Ferrell et al., 1981, 1985; Hill and
Almli, 1980; Hosley and Oakley, 1987; Mistretta, 1972;
Yamada, 1980). Furthermore, criteria for bud counting
did not rely exclusively on the presence of a taste pore.
Thus, even if the pore region were obscured by oblique
sectioning, or resisted staining after denervation (Hou
et al., 19851,the bud would still be counted if identified
by other characteristics (see below).
MATERIALS AND METHODS
Surgery was performed on six female SpragueDawley rats ranging in age from 28 to 35 days (mean
age = 30 days; mean weight = 86 g). The rats were
anesthetized (Equithesin) and placed in a supine position for a ventral approach to the nerve. The head was
stabilized via a rubber band extending from just behind
the incisor teeth to a cardboard box containing the body
warmer.
A skin incision was made just lateral t o the midline
and parallel to the mandible. Blunt dissection exposed
the posterior belly of the digastricus, styloglossus, internal pterygoid, and masseter muscles (see Greene,
1955) that were then retracted. The chorda tympani
nerve was visualized as it passed ventral to the lateral
pterygoid plate and into the tympanic bulla. A length
of nerve was exposed, cut distally, and evulsed proximally (n = 2) with jeweler’s forceps. No muscles were
cut. The chorda tympani is still undergoing the process
of myelinization at this age (Ferrell et al., 1985) and is
delicate, and difficult to locate, thereby necessitating
an alternative surgical approach. Since the rat chorda
tympani has its origin in the facial nerve canal (Green
19551, about a 6 mm length of facial nerve was evulsed
(n = 4) as it exited the adjacent stylomastoid foramen.
This portion of extirpated nerve included the chorda
tympani and remnants of geniculate ganglion cells
(verified histologically in some cases). In all cases, a
10% (wt/vol) solution of methyl methacrylate polymer
(Howe & French, Boston) was applied to the distal cut
end of the nerve, petrotympanic fissure, andlor stylomastoid foramen. At this concentration, transected
nerves coated with methyl methacrylate fail to regenerate even after 1 year (Edds, 1945).
After postsurgical intervals of 30, 45, 60, 75, and 90
days, animals were deeply anesthetized and perfused
transcardially with 0.9% saline followed by 10% neutral formol-saline. The tongues were removed and
stored in formol-saline, and the success of surgery was
confirmed by dissection. The anterior-most 2-3 mm of
the tongue was dehydrated, embedded in paraffin, and
serially sectioned in the frontal plane (7-10 pm). Successive 100 km distances of tissue were alternately
stained with hematoxylin and eosin, cresyl violet, and
Pollak‘s trichrome stain (Humason, 1972). Iron hematoxylin was used in one additional case, but found to be
the least useful and discontinued.
All sections were examined serially by two independent observers, who were unaware on which side the
surgery was performed or of the survival times.
Rat fungiform papillae typically contain a single
taste bud. In light microscopy, these buds have four
main characteristics: 1)dorsally, a pore opens into the
oral cavity; 2) the cytoplasm of bud cells stains dif-
Fig. 1. Comparison of taste papillae contralateral and ipsilateral
to gustatory neurectomy a t various survival times. Calibration bar: A
= 100 pm, B = 16 pm, C = 27 pm, D = 41 pm, E = 26 pm. A: Two
fungiform papillae (arrows) in the midline region of the anterior dorsal surface of the tongue. Asterisk is located within the lingual central sulcus. Papilla on the right is contralateral to neurectomy and
contains a taste bud. Surgery, 35 days; survival time, 90 days; cresyl
violet stain. B: Intact fungiform taste bud, contralateral to gustatory
neurectomy. Surgery, 31 days; survival time, 75 days; cresyl violet
stain. C: A budless fungiform papilla ipsilateral to gustatory neurectomy. Surgery, 35 days; survival time, 90 days; cresyl violet stain. D:
Fungiform papilla, ipsilateral to gustatory neurectomy, whose dorsal
surface is keratinized and bears a filiform-like peak. Surgery, 35 days;
survival time, 90 days; Pollak trichrome stain. E: Fungiform papilla
ipsilateral to gustatory neurectomy, with a n ovoid, cell aggregate
(arrow) in its dorsal epithelium. Surgery, 28 days; survival time, 45
days; hematoxylin and eosin stain.
CHORDA TYMPANI NEURECTOMY
Fig. 1
227
228
J.R. GANCHROW AND D. GANCHROW
ferently from the surround (usually lighter); 3) the orientation of bud cells is mainly perpendicular to the
surface in contrast to the horizontal layering of surrounding epithelial cells; on the lateral edges of the
buds-in-longitudinal-section, cellular organization is
less well-defined, but still not horizontal; and 4) the
basal region of the bud invaginates the underlying papillary connective tissue core. The occasional budless
papilla has an uninterrupted basal cellular layer. In
order not t p overlook buds on the operated side, observation of any one of these signs on either side was
accepted as a potential bud, the structure traced serially, and counted.
RESULTS
About 80% of the contralateral (unoperated side), as
compared with 12% of the ipsilateral (operated side),
fungiform papillae contained buds or budlike formations. The number of taste buds counted on the unoperated side ( n = 247) greatly exceeded that on the operated side (n = 26) regardless of age or surgical
approach (see Table 2). In the midline region, ipsilaterally, 18 structures mostly displayed all four bud
characteristics as described in the Materials and Methods section. The remaining eight, more laterally situated budlike structures on the operated side appeared
as small cell clusters in the basal epithelium of the
dorsal surface of the papilla (see below).
Figure 1compares taste buds on the unoperated and
operated sides. Figure 1A shows two fungiform papillae (arrows) flanked by several stalklike filiform papillae in the lingual midline region. The fungiform papilla on the unoperated side (right) contains a normal,
onion-shaped taste bud that, when traced serially, exhibited all four defining bud features (see Materials
and Methods). In contrast, the fungiform papilla on the
operated side (left) is budless. At a higher magnification, Figure 1B demonstrates that the fungiform bud in
nonneurectomized tissue is easily discernible from the
stratified epithelial surround in that the bud contains
lighter-staining, vertically oriented cells with large,
round nuclei. Moreover, a taste pore opens from the
apical bud region, and a sheath of darker-staining cells
surrounds the basal two-thirds of the bud, which in
turn, invaginates the connective tissue core. None of
these features are observed in most fungiform papillae
ipsilateral to gustatory neurectomy.
Figure 1C illustrates a typical fungiform papilla deprived of gustatory innervation. The basal epithelial
cell layer overlaying the connective tissue core is uniform and uninterrupted. Some darkly stained cells appear to lie above the most basal stratum in the central
apical region of the papilla, but this epithelial organization does not resemble that of a taste bud.
Following surgery on the operated side, some broad
fungiform papillae reflect filiform structure. For example, in Figure lD, papillary width suggests a fungiform
characteristic but for a miterlike protuberance near
the dorsal center of the papillar epithelium. Moreover,
the oral surface of this papilla is unusually well keratinized. Though noted several times, the frequency of
this combining papillar form was not specifically
counted.
Figure 1E shows a fungiform papilla ipsilateral to
gustatory neurectomy and presents the best of eight
examples of structures counted as budlike from the lateral edge of the tongue (Table 2). Near the dorsal center of the papilla, in the basal epithelium, a cell aggregate (arrow) with large darkly staining nuclei appears
to barely invade the connective tissue ventrally and
dorsally extends toward but does not penetrate through
overlying stratified epithelium t o reach the papillar
surface. Cytoplasm of this cell cluster stained similarly
to that of cells in the epithelial surround, and there was
no particular vertical cell organization characteristic of
mature buds. Keratin covering the papillar dorsal surface was similar to that in adjacent tissue. This aggregate, at best, resembles the embryonic “spherical
stage” of (presumptive) taste bud development prior to
pore communication with the oral cavity (cf., Bradley
and Stern, 1967; Bradley et al., 1980; Mistretta, 1972;
Ganchrow and Ganchrow, 1987) and was equally discernible with each of the histologic stains used. The
slight bulge into the connective tissue core was a consistent feature of these budlike structures.
Lastly, some fungiform papillae ipsilateral to neurectomy appeared to be smaller than those contralaterally. Furthermore, ipsilaterally, the number of
clearly definable fungiform papillae diminished by
about 30%. Atrophic signs in foliate and circumvallate
papillae have also been reported (e.g., Guth, 1963;
Naga et al., 1970, von Vintschgau and Honigschmied,
1877; Zalewski, 1969a) following gustatory nerve
transection.
DISCUSSION
Surgical destruction of the chorda tympani nerve in
1month-old rats nearly eliminated all taste buds in the
ipsilateral fungiform papillae. With the most lenient of
bud definitions, the operated side of the anterior-most
lingual surface contained about one-tenth as many
buds as seen contralaterally. More than half of this
small, ipsilateral bud population was located near the
lingual midline and displayed mature bud features.
This raises the question of whether fungiform papillae
near the median plane are normally bilaterally or contralaterally innervated.
Normal bilateral innervation is evident for taste
buds in the rat circumvallate papilla (e.g., Guth, 1963;
Hosley et al., 1987; Oakley, 1974; Whiteside, 1927).
Zander (18971, using gross dissection techniques in human cadavers, reported that fibers of the lingual
branch of the trigeminal nerve (in which the distal
chorda tympani passes) also cross the midline, especially in the anterior-most 5 mm of lingual tissue. In
gerbils, Cheal and Oakley (1977) unilaterally removed
the chorda tympani nerve, producing ipsilateral taste
bud degeneration, and then performed a contralateral
chorda tympani neurectomy. They concluded that
“with the possible exception of a few fungiform papillae
on or adjacent to the midline, all taste bud innervation
in the foliate and fungiform papillae is ipsilateral” (p.
613). Likewise, following lingual neurectomy in the
kitten (Hayes and Elliott, 1942) and adult rat (Whiteside, 19271, taste buds were seen in fungiform papillae
229
CHORDA TYMPANI NEURECTOMY
TABLE 2. Taste bud counts for various survival times following chorda tympani (CT) or
facial nerve (FN)neurectomy
Neurectomv
CT
CT
FN
FN
FN
FN
Age
at
surgery
(davs)
25
34
28
29
31
35
Survival
time
(days)
30
60
45
60
75
90
Tongue
length
sampled
(mm)
2.0
2.0
2.6
2.6
2.4
2.9
located in the ipsilateral “midregion,” especially a t the
tongue tip. Whether this is the normal situation, or
contralateral sprouting induced by denervation had occurred, is a research question that to date has not been
adequately addressed. Recently, Hou et al. (1985) recorded from the hamster intact chorda tympani following unilateral chorda tympani removal. They concluded that “no chorda tympani contralateral to
neurectomy responded to chemical stimulation localized to the side of the tongue ipsilateral to neurectomy,
indicating numerous fibers had not sprouted across the
midline” (p. 444). It is unclear whether 1) the most
medial fungiform papillae of the anterior tongue were
stimulated in this study or 2) a critical number of midline papillae must be stimulated to assure adequate
responsiveness of the intact chorda tympani.
What of that small population of cell aggregates seen
after ipsilateral neurectomy that lie in basal epithelium of fungiform papillae, lateral to the midline region? As reported here in the young rat, these aggregates appear substantially less well organized than the
buds described in adult hamster after gustatory nerve
transection (Whitehead et al., 1987). Possibly, the cell
aggregates may constitute the remnants of the last degenerating buds following denervation or simply are
thickenings of the dorsal, central fungiform epithelium
whose cells are oriented in nonlaminar fashion. If the
first hypothesis was correct, progressive degenerative
changes across survival times might have been expected, but were not observed. Alternatively, some cellular aggregates observed in the dorsal epithelium of
fungiform papillae deprived of gustatory innervation
could represent an epithelial reorganization, not unlike that in filiform papillae (Farbman, 1970). Two of
the eight budlike structures were found in papillae exhibiting a slight peak a t the dorsal surface (cf. Fig. 1D).
Finally, recent evidence from adult rats has suggested
that lingual nerve collateral sprouting may be able to
reinnervate some taste buds that have sustained
chronic chorda tympani resection (Kinnman and Aldskogius, 1988).
With the exception of a few midline-region buds, the
present study using relatively long survival times in
young rats failed to reveal any mature taste buds ipsilateral to the neurectomies that were comparable to
the well-developed examples reported for the mature
hamster (Whitehead et al., 1987). This difference may
have been related to bud-nerve ontogenetic factors occurring coincident with the experimental time frame of
Unoperated
side
29
41
56
37
34
50
Taste bud counts
Operated side
Midline area
More lateral
1
2
3
1
7
3
0
1
3
0
4
1
our prepubertal animals. Hosley et al. (1987) examined
the ability of circumvallate taste buds to be induced
following glossopharyngeal nerve transections in rats
whose ages included those used in the present study.
While the greatest retardation to induction was observed following nerve transections in the first 10 postnatal days, the capacity for taste bud induction was
still impaired when transection was carried out at 30
postnatal days. Possibly, complete replacement of a degenerated bud is dictated by a site previously occupied
by a mature bud. Mature circumvallate taste buds increase their numbers up to 90 postnatal days (Hosley
and Oakley, 1987). To our knowledge, a complete developmental time course for fungiform taste bud maturation in the rat has not been quantified, although
Hill (1987) suggests it probably continues through the
first postnatal month since maturation of chorda tympani nerve responsiveness extends well beyond this period. Perhaps the capacity to form or maintain a bud
following sustained neurectomy may require animals
older than those used in the present study. It might be
pointed out that the population of hamster fungiform
taste buds does not increase between 19 and 140 postnatal days (Miller and Smith, 1984).
In conclusion, the postlesion persistence or development de novo of the peripheral gustatory receptor in
some adult vertebrate forms may indicate the strength
of local factors guiding the expression of taste neuroepithelium in mature animals. Taste bud ontogenesis in
younger animals may be more critically neurally dependent. A longer survival period per se does not appear to be the major determining factor of taste bud
survival.
ACKNOWLEDGMENTS
This research was supported, in part, by a grant from
the United States-Israel Binational Science Foundation (B.S.F.),Jerusalem, Israel. We would like to thank
Joan Hamilton, Steve Hutchison, and Paul Gustafson
for their technical assistance, Asher Pinchasov for photographic expertise, Dr. Paul Haas for translating German literature relevant to the research problem, Shula
Konig for typing the manuscript, and the reviewers for
constructive criticisms.
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