Target pioneering and early morphology of the murine chorda tympani
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1 J. Anat. (1998) 192, pp , with 3 figures Printed in the United Kingdom 91 Target pioneering and early morphology of the murine chorda tympani LISA SCOTT AND MARTIN E. ATKINSON Department of Biomedical Science, University of Sheffield, UK (Accepted 30 September 1997) ABSTRACT Many studies demonstrate that differentiation of certain sensory receptors during development is induced by their nerve supply. Thus the navigational accuracy of pioneering fibres to their targets is crucial to this process. The special gustatory elements of the facial and glossopharyngeal nerves are used extensively as model systems in this field. We examined the chorda tympani, the gustatory component of the facial nerve, to determine the precise time course of its development in mice. The transganglionic fluorescent tracer DiI was injected into the anterior aspect of the mandibular arch of fixed embryos aged between 30 and 50 somites (E10 E12). It was allowed to diffuse retrogradely via the geniculate ganglion to the brainstem for 4 wk, before the distribution of DiI was determined using confocal laser scanning microscopy. Geniculate ganglion cells were first labelled at the 34 somite stage (E10). Pioneering chorda tympani fibres that arise from these cells passed peripherally and followed an oblique course as they grew towards the mandibular arch. At the 36 somite stage (E10.5), the peripheral component followed an intricate postspiracular course and passed anteriorly to arch over the primitive tympanic cavity, en route to the lingual epithelium. From the 36 to 50 somite stages (E10 5 E12), it consistently traced in the fashion of a U bend. The central fascicle also traced at the 36 somite stage (E10 5) and just made contact with the brainstem. At the 40 somite stage (E11), the central fibres clearly chose a route of descent into the spinal trigeminal tract and branched into the solitary tract. Pioneering chorda tympani fibres contact the lingual epithelium when the target is primordial. The lingual epithelium may be a source of a neurotropic factor that attracts peripheral chorda tympani fibres to the sites of putative papillae. However, the chorda tympani is probably not a vital influence on the subsequent differentiation of gustatory papillae, since the papillae are elaborated 5 d later at E15 in murine embryos. The early morphology of the nerve is true to the amniote vertebrate phenotype. Key words: Facial nerve; gustatory papillae. INTRODUCTION The first pioneer axons to approach their correct targets appear to know their home address during early phases of axogenesis. Some pioneers traverse considerable distances, coursing through various substrates and bypass several organs en route, but remain committed to their natural target. Soluble factors released by neuronal target tissues are involved in the formation of normal neural networks. For example, in the trigeminal system, explants of placode-derived trigeminal ganglion neurons of the chick produce neurites in the presence of brain-derived neurotrophic factor (BDNF) (Davies et al. 1986). In the gustatory system, BDNF mrna is detectable in both the fungiform and circumvallate papillae of the developing rat tongue. Its appearance coincides with lingual epithelium innervation but is prior to the formation of taste buds (Nosrat & Olson, 1995). BDNF may therefore function as a targetderived chemoattractant to the special gustatory neurons. The navigational fidelity of sensory axons to their targets is also crucial to the normal development of certain sensory receptors. For example, the glossopharyngeal nerve induces taste bud formation in rat Correspondence to Dr Martin Atkinson, Department of Biomedical Science, University of Sheffield, Alfred Denny Building, Western Bank, Sheffield S10 2TN, UK.
2 92 L. Scott and M. E. Atkinson Mdc Bs Op Md Mx Md Hy 1a VII CTp 1b Fig. 1. (a) Fluorescence microscopy of the murine chorda tympani traced with DiI from the anterior aspect of the mandibular arch of a fixed mouse embryo at 34 somites (E10). The peripheral axons (CTp) exit the geniculate ganglion (VII) and pass obliquely through the hyoid arch towards the mandibular arch. Thus the initial axogenesis from the geniculate ganglion extends peripherally and not centrally. DiI also labelled the mandibular nerve via peripheral axons and the mandibular component of the trigeminal ganglion (Md). The central axons (MdC) contacted the brainstem (Bs). The close relationship between the mandibular trigeminal ganglion and the geniculate ganglion is evident. 100 (b) Camera lucida drawing of an E10 5 mouse embryo redrawn from Davies & Lumsden (1984) to illustrate the regional anatomy of the trigeminal and facial nerves. The ophthalmic nerve (Op) and the maxillary (Mx), mandibular (Md) and hyoid (Hy) arches are shown with their associated cranial nerves. Chorda tympani arrowed. The red box surrounds the region of the head that is captured in Figure 1a. posterior lingual epithelium postnatally (Hosley et al a). Denervation from postnatal d 0 to 10 produces an impairment of taste bud formation (Hosley et al b). Nongustatory vagal afferents are capable of reinnervating a denervated tongue and restore normal morphology to the taste buds (Zalewski, 1981). Therefore, the neural induction signal is not unique to the normal gustatory afferents. Similarly, the gustatory afferents of the neonatal rat chorda tympani, which normally innervate taste buds on the anterior tongue, will also support circumvallate taste buds on the posterior tongue (Oakley, 1993). In the fetal rat, there is evidence for an initial neurotropic effect from the anterior lingual epithelium (on the chorda tympani and lingual branch of the trigeminal nerve) and the epithelial cells of the fungiform papillae apex (on the chorda tympani only). Initial morphogenesis of the fungiform papillae commences in the absence of any neural influence but the rat chorda tympani may induce the differentiation of taste buds on the papillae (Farbman & Mbiene, 1991). The long-term rabbit neurectomy studies of Nakashima et al. (1990) demonstrate that once the receptor-nerve cell relationship is established, the fungiform papillae become trophically dependent on the neurons. Within the trigeminal system of the rat, peripheral and central axons of the trigeminal ganglion show a spatial order on reaching the vibrissal field at E12 and the brainstem at E13 respectively. These events are prior to the differentiation of the sensory end-organs, vibrissae follicles and brainstem trigeminal nuclei (Erzurumlu & Jhaveri, 1992). The studies outlined above suggest the operation of
3 Development of the chorda tympani 93 Fig. 2. Confocal laser scanning image with a phase-contrast image of the same field overlaid. In this 36 somite specimen (E10 5) transganglionic tracing of DiI from the anterior aspect of the mandibular arch of a fixed mouse embryo has labelled central (CTc) and peripheral (CTp) chorda tympani axons and their cell bodies (Cb) in the geniculate ganglion. The morphology of the chorda tympani is defined by the posterior relation to the spiracle (Sp) and the anterior relation to the tympanic cavity (TC). The spiracular epithelium (Ep) and the tympanic cavity were discernible using phase-contrast microscopy. DiI also labelled the mandibular component of the trigeminal ganglion (Md) via the peripheral fascicle (P) a vital intrinsic influence governing the phenotype of pioneer neurons. Consequently, in particular receptornerve cell systems, such neurons exert profound effects on the differentiation of their sensory end-organs. Kuratani et al. (1988) described the morphology of the chorda tympani during chick development. Using an immunohistochemical staining technique, they revealed both prespiracular (stage 17) and postspiracular (stage 21) components of the chorda tympani, which together encircled the spiracle (the upper part of the first branchial groove). This so called spiracular loop appears to be unique to the chick since Goodrich (1914) demonstrated that the chorda tympani in amniote vertebrates is entirely postspiracular. The aim of the present study is to examine the course of developing peripheral and central chorda tympani axons and the time that they pioneer their respective targets. From our experimental data it is possible to speculate upon the importance of targetderived chemotropic influences and the inductive
4 94 L. Scott and M. E. Atkinson relationship between axons and their sensory receptors. MATERIALS AND METHODS Pregnant time-mated MF mice between 10 and 12 d of gestation were killed by cervical dislocation. The presence of a vaginal plug was designated as E0. The uteri were removed and placed in phosphate buffered saline (ph 7 2). The embryos were dissected from the uteri and extraembryonic membranes then accurately aged by both external morphological criteria and by somite counts (Theiler, 1989). The embryos were decapitated immediately and the heads fixed in a solution of phosphate buffered 4% paraformaldehyde and 0 2% glutaraldehyde (ph 7 2) for 1 d at room temperature. Crystals of the fluorescent carbocyanine neuronal tracer DiI [1,1 -dioctadecyl-3,3,3,3 -tetramethylindocarbocyanine percholate; DiI-C18-(3)] (Molecular Probes Oregon, USA) were dissolved in dimethylformamide (1 5 mg in 200 µl). Small quantities of solution were drawn up by capillary action into heat stretched glass micropipettes, which were used to insert the tracer. DiI was injected unilaterally into the anterior aspect of the right mandibular arch in 30 to 50 somite stage embryos (E10 E12) to trace the peripheral and central components of the mandibular nerve and the chorda tympani to the brainstem. In all cases, suction of excess fluid out through the stomodeum by micropipette capillary action prevented spread of tracer to other areas. Successful placement of tracer into the correct target area was monitored by a primary examination using an inverted Leitz fluorescence microscope equipped with TRITC filters. When the correct location of the tracer was confirmed, the injected heads were returned to fixative in 2 ml eppendorf tubes. These were wrapped in aluminium foil to prevent photobleaching. The tissues were stored at room temperature in the dark for between 1 and 4 wk to allow the tracer to diffuse retrogradely. After 1 4 wk, each head was bisected in the sagittal plane and the distribution of the tracer in the right half observed using fluorescence microscopy in combination with phase-contrast microscopy. Each specimen was mounted in PBS on a 35 mm tissue culture dish, with the lateral aspect of the bisected head placed inferiorly. Photomicrographs were taken on Kodak Gold 200 colour print film and this was developed and printed routinely. Several specimens received more detailed examination. These were mounted beneath a coverslip in PBS on a well slide, with the lateral aspect of the bisected head placed superiorly. Optical sections were obtained at 2 22 µm intervals to a maximum depth of 176 µm using an upright Leica TCS 4D confocal laser scanning microscope set up for observation of DiI. A standard TRITC filter set was used and each specimen was excited at 568 nm with a 590 nm low pass emission filter (Honig & Hume, 1989). Between 8 and 16 full frame images (512 by 512 pixels) were collected and stored for each specimen. These images were further processed using the manufacturer s software so that serial sections were stacked to give extended focus views. The colour of the tracer was then assigned electronically to give the characteristic appearance of red-orange DiI. Phase-contrast images were obtained on the CLSM using a detector mounted beneath the condenser set up with appropriate rings. Fluorescence and phasecontrast images were overlaid to define the chorda tympani in relation to the spiracle and the tympanic cavity. The final images were sized and labelled using the Micrografx Picture Publisher LE 4.0a programme. A Lasergraphics slide maker transferred the electronic images onto Kodak Gold 100 colour print film and this was developed and printed routinely. RESULTS (see Table) somites (E10) There was no labelling of chorda tympani axonal processes or geniculate ganglion cell bodies between 30 and 33 somite stages. DiI was restricted to the insertion site, although secondary transcellular labelling was detectable in the surrounding mesenchyme (data not shown) somites ( ) The chorda tympani was first labelled at this stage. Only the peripheral fascicle traced with DiI from the mandibular arch to the geniculate ganglion (Fig. 1 a). The fascicle exited from the peripheral aspect of the ganglion and passed obliquely through the hyoid arch towards the mandibular arch. Only 2 3 neurons were present in all speciemens examined. No central fibres were discernible, which indicates that the initial axogenesis from the geniculate ganglion extends peripherally and not centrally. In addition to the chorda tympani, the mandibular nerve traced at the 34 somite stage. DiI was transported retrogradely to the brainstem in peripheral and central axons of bipolar neurons via the mandibular component of the trigeminal ganglion
5 Development of the chorda tympani 95 (Fig. 1a). Figure 1b illustrates the lateral aspect of an E10 5 mouse embryo to demonstrate the regional anatomy of the trigeminal and facial nerves. 36 somites (E10 5) In addition to the peripheral fascicle, the centrally oriented fascicle of the chorda tympani (a component of the nervus intermedius) traced at this stage. Consequently, the complete first order pathway composed of bipolar neurons was discernible for the first time (Fig. 2). This central outgrowth travelled a short distance from the geniculate ganglion to make a direct contact with the brainstem. The peripheral fascicle passed downwards and beneath the spiracular epithelium to follow a posttrematic course into the hyoid arch. It passed posterior and inferior to the spiracle and thence continued anteriorly and superiorly, arching over the posterior aspect of the primitive tympanic cavity towards the mandibular arch, creating a U-bend en route. In all somite specimens examined, only 2 8 pioneering chorda tympani neurons were visible somites (E10 5) The morphology of the chorda tympani continued as described above except the U-bend developed a more acute curve. The peripheral and central fascicles became progressively more robust but accurate neuron counting was no longer possible since the fibres were intermingled and compacted. The central fascicle gradually descended further into spinal trigeminal tract. 40 somites (E11) The peripheral axons of the chorda tympani arose from the peripheral aspect of the geniculate ganglion and at an approximate right angle to the central fascicle (Fig. 3 a, b). The central fascicle branched so that fibres distributed to the spinal trigeminal tract and also to the domain of the tractus solitarius, which lies dorsal to this tract (Fig. 3a, c). It is likely that the branch to the tractus solitarius contains the special visceral afferents for taste. The axons entering the spinal trigeminal tract are possibly general somatic afferents of the facial nerve. The latter vary enormously between individuals and behave like the afferents of the trigeminal nerve once in the spinal trigeminal tract (Nolte, 1993) somites (E11 E12) The complete chorda tympani tracing was reproducible without deviation throughout these stages. In the age ranges examined, the peripheral component of the chorda tympani did not fasciculate with the neighbouring mandibular division of the trigeminal nerve. Figure 1 a shows a general view of the relationship between the mandibular division of the trigeminal ganglion and the geniculate ganglion, with the associated axonal processes present at the 34 somite stage (E10). The results are summarised in the Table. DISCUSSION This in vivo dye tracing study demonstrates that pioneer peripheral axons in the chorda tympani reach the lingual epithelium at the 34 somite stage (E10). This projection is the first outgrowth from the geniculate ganglion and the central fascicle arises 2 somite stages later. The early morphology of the chorda tympani corresponds to the characteristic amniote vertebrate design. Axons did not trace at the somite stages (E10). This indicates either the absence of axonal projections from the chorda tympani or that pioneering neuron had not reached the source of the tracer by this time. It is therefore possible that pioneering axons had embarked on their journey to the periphery during this time but were not traceable in these early stages. At the 34 somite stage (E10), the peripheral component of the chorda tympani traced for the first time. It followed an oblique route to the mandibular arch, which was relatively direct when compared with later stages. The subsequent tortuous course of the nerve appears to be secondary to the dynamic sculpting of the branchial region of the head and is not convoluted orienteering. The central component of the chorda tympani traced 2 somite stages later at the 36 somite stage (E10 5). The development of the chorda tympani is truly outside-in since the central projection arises subsequent to the initial peripheral axogenesis. This result contrasts the early pioneering behaviour of the murine trigeminal system in which the maxillary and mandibular nerves simultaneously extend axons both peripherally and centrally (Scott & Atkinson, unpublished). This outside-in sequence conforms to the development of the gustatory pathways at higher levels. For example, dendrites of neurons in the rat rostral nucleus of the solitary tract ramify extensively between postnatal d 6 and 20. During this period the volume of the chorda tympani
6 96 L. Scott and M. E. Atkinson Fig. 3. Confocal laser scanning images to show transganglionic tracing of DiI from the anterior aspect of the mandibular arch of a fixed mouse embryo at 40 somites (E11). (a) The peripheral axons of the chorda tympani (CTp) arise from the geniculate ganglion (VII) at an approximate right angle to the central axons (CTc). The central fascicle branches so that fibres distribute to the long spinal trigeminal tract (SpV) and to the domain of the tractus solitarius (Br) (b) Higher magnification image of the cell body detail in the geniculate ganglion (c) Higher magnification image of the branch to the tractus solitarius with the zoom option applied terminal field doubles in the nucleus of the solitary tract (Lasiter et al. 1989). Furthermore, synapse and dendrite development in the rat parabrachial gustatory zone at the second order level occurs simultaneously between postnatal d 18 and 35. This event follows morphological development in the first order pathway and the rostral nucleus of the solitary tract (Lasiter & Kachele, 1988, 1989, 1990). Outside-in development also reflects the trophic dependence of the central projection on the intact peripheral projection in adult rodents. For example, severance of the hamster chorda tympani induces degeneration of the central terminals in the nucleus of the solitary tract. This degeneration arises from altered synaptology and not ganglionic cell death (Whitehead et al. 1995). Therefore, the finding that peripheral projections develop prior to their central counterparts strengthens the evidence that anatomical integrity and physiological health are crucial to the maintenance of gustatory competence in adulthood. Gross innervation of murine lingual mucosa is well established by E12 but gustatory papillae do not appear until E15 (Nolte & Martini, 1992) and taste bud differentiation in circumvallate papillae commences on d 0 after birth (Takeda et al. 1992). The 5 d time lag between pioneering innervation of lingual epithelium at E10 and appearance of the papillae makes it highly unlikely that nerves induce papilla
7 Development of the chorda tympani 97 Table. Summary of results Age of embryo Retrograde dye tracing* Embryonic day Somite count CTp CTc Sp Br E E E E12 50 * CTp, peripheral axons of chorda tympani traced from anterior aspect of mandibular arch to geniculate ganglion. CTc, central axons of chorda tympani traced transganglionically from anterior aspect of mandibular arch to contact brainstem. Sp, chorda tympani passed posterior to spiracle and anterior to tympanic cavity en route to the mandibular arch. Br, chorda tympani entered tractus solitarius and some axons progressively descended further into spinal tract. formation and differentiation. Furthermore, there is recent evidence that gustatory papillae develop without neural influence. Organ cultures of embryonic rat tongue show normal papillary spatiotemporal differentiation (Mbiene et al. 1997). There is also striking evidence that BDNF is preferentially expressed in putative gustatory areas of the lingual epithelium prior to and during papillary differentiation and formation (Nosrat & Olson, 1995; Nosrat et al. 1996). BDNF may function as a short range chemotropic mechanism to delineate innervation of papillae from subepithelial plexuses, since in BDNF null mutant mice, taste bud formation and their intraepithelial innervation is impaired (Nosrat et al. 1997). The factors that direct the initial axogenesis of peripheral and central chorda tympani projections when they arise from the geniculate ganglion remain elusive. Nevertheless, it is apparent from our study that an initial chemotropic influence from the murine target tissue could take effect when the target is in premature stages of differentiation before the 34 somite stage (E10). Therefore, putative tropic factors are likely to be regionally attractive and not specifically attractive to guide axon terminals to sensory endorgans. In the present study, the peripheral fascicle adopted the characteristic morphology of the chorda tympani at the 36 somite stage (E10.5). The tracing pattern was replicated up to the 50 somite stage (E12). Kuratani et al. (1988) presented an anatomical definition of the chick chorda tympani using its relation to the spiracle and the tympanic cavity as defining factors. DiI tracing revealed that the peripheral fascicle of the murine embryo passes posterior to the spiracle and progresses downward into the hyoid. It then turns upward forming a U-bend that arches over the posterior aspect of the tympanic cavity, before continuing anteriorly to the tongue. The chorda tympani in the murine embryo is therefore postspiracular. This contrasts with the arrangement in the chick, in which the nerve is mostly prespiracular with a less robust postspiracular branch. Together, these 2 branches form a loop that encircles the spiracle (Kuratani et al. 1988). The general morphology of the chorda tympani in the present study is consistent with the fundamental observation that the chorda tympani always locates between mandibular and hyoid skeletal elements (Gaupp, 1912, cited by Kuratani et al. 1988). More specifically, the murine chorda tympani is entirely postspiracular, conforming to the more usual arrangement in amniote vertebrates (Goodrich, 1914). The mandibular nerve and the chorda tympani did not appear to fasciculate in the periphery at any of the embryonic stages studied in this investigation. However, the extreme peripheral courses of the mandibular nerve and the chorda tympani were masked by the injection site. Therefore, fasciculation at their extremities is a possibility. Nevertheless, numerous photomicrographs and camera lucida drawings of murine cranial nerve development in the literature do not show fasciculation of the mandibular nerve and the chorda tympani at E10 E11 (see, e.g. Davies & Lumsden, 1984, fig. 1; Meyer & Birchmeier, 1995, fig. 4). In conclusion, the murine chorda tympani is postspiracular and pioneers the lingual epithelium at the 34 somite stage (E10) via a relatively direct route. The intricate morphology of the nerve at the 36 somite stage (E10 5) is not convoluted orienteering but is secondary to the sculpting of the branchial region of the head. The undifferentiated lingual epithelium may be a source of a chemotropic factor that facilitates chorda tympani navigational success once it has proceeded distal to the developing outer and middle ear cavities. Considering that the lingual papillae develop following the initial innervation of the tongue, chorda tympani nerve fibres are not dependent on their sensory end-organs for guidance. Due to the considerable time-lag between lingual innervation and papillary differentiation, the nerve supply evidently does not induce morphological changes in the lingual epithelium at the early pioneering stage, confirming the observations of Farbman & Mbiene (1991).
8 98 L. Scott and M. E. Atkinson ACKNOWLEDGEMENTS The authors thank Dr Adrian Jowett for assistance with the operation of the confocal laser scanning microscope and production of the final images. The microscope was funded by the Wellcome Trust. This study was supported by a scholarship awarded to Lisa Scott by the Anatomical Society of Great Britain and Ireland. REFERENCES DAVIES A, LUMSDEN A (1984) Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion. Journal of Comparative Neurology 223, DAVIES AM, THOENEN H, BARDE Y-A (1986) The response of chick sensory neurons to brain-derived neurotrophic factor. Journal of Neuroscience 6, ERZURUMLU RS, JHAVERI S (1992) Trigeminal ganglion cell processes are spatially ordered prior to the differentiation of the vibrissa pad. Journal of Neuroscience 12, FARBMAN AI, MBIENE J-P (1991) Early development and innervation of taste bud-bearing papillae on the rat tongue. Journal of Comparative Neurology 304, GOODRICH ES (1914) The chorda tympani and middle ear in reptiles, birds, and mammals. Quarterly Journal of Microscopical Science 61, HONIG MG, HUME RI (1989) DiI and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends in Neurosciences 12, HOSLEY MA, HUGHES SE, OAKLEY B (1987a) Neural induction of taste buds. Journal of Comparative Neurology 260, HOSLEY MA, HUGHES SE, MORTON LL, OAKLEY B (1987b) A sensitive period for the neural induction of taste buds. Journal of Neuroscience 7, KURATANI S, TANAKA S, ISHIKAWA Y, ZUKERAN C (1988) Early development of the facial nerve in the chick embryo with special reference to the development of the chorda tympani. American Journal of Anatomy 182, LASITER PS, KACHELE DL (1988) Postnatal development of the parabrachial gustatory zone in rat: dendritic morphology and mitochondrial enzyme activity. Brain Research Bulletin 21, LASITER PS, KACHELE DL (1989) Postnatal development of protein P-38 ( Synaptophysin ) immunoreactivity in pontine and medullary gustatory zones of rat. Developmental Brain Research 48, LASITER PS, WONG DM, KACHELE DL (1989) Postnatal development of the rostral solitary nucleus in rat: dendritic morphology and mitochondrial enzyme activity. Brain Research Bulletin 22, LASITER PS, KACHELE DL (1990) Effects of early postnatal receptor damage on development of gustatory recipient zones within the nucleus of the solitary tract. Developmental Brain Research 55, MBIENE J-P, MACALLUM DK, MISTRETTA CM (1997) Organ cultures of embryonic rat tongue support tongue and gustatory papilla morphogenesis in vitro without intact sensory ganglia. Journal of Comparative Neurology 377, MEYER D, BIRCHMEIER C (1995) Multiple essential functions of neuregulin in development. Nature 378, NAKASHIMA T, TOYOSHIMA K, SHIMAMURA A, YAMADA N (1990) Morphological changes of taste buds and fungiform papillae following long-term neurectomy. Brain Research 533, NOLTE J (1993) The Human Brain (An Introduction to its Functional Anatomy), 3rd edn, p St Louis: Mosby Year Book. NOLTE C, MARTINI R (1992) Immunocytochemical localization of the L1 and N-CAM cell adhesion molecules and their shared carbohydrate epitope L2 HNK-1 in the developing and differentiated gustatory papillae of the mouse tongue. Journal of Neurocytology 21, NOSRAT CA, OLSON L (1995) Brain-derived neurotrophic factor mrna is expressed in the developing taste bud-bearing tongue papillae of rat. Journal of Comparative Neurology 360, NOSRAT CA, EBENDAL T, OLSON L (1996) Differential expression of brain-derived neurotrophic factor and neurotrophin 3 mrna in lingual papillae and taste buds indicates roles in gustatory and somatosensory innervation. Journal of Comparative Neurology 376, NOSRAT CA, BLOMLO F J, ELSHAMY WM, ERNFORS P, OLSON L (1997) Lingual deficits in BDNF and NT3 mutant mice leading to gustatory and somatosensory disturbances, respectively. Development 124, OAKLEY B (1993) The gustatory competence of the lingual epithelium requires neonatal innervation. Developmental Brain Research 72, TAKEDA M, SUZUKI Y, OBARA N, NAGAI Y (1992) Neural cell adhesion molecule of taste buds. Journal of Electron Microscopy 41, THEILER K (1989) The House Mouse (Atlas of Embryonic Development). New York: Springer. WHITEHEAD MC, MCGLATHERY ST, MANION BG (1995) Transganglionic degeneration in the gustatory system consequent to chorda tympani damage. Experimental Neurology 132, ZALEWSKI AA (1981) Regeneration of taste buds after reinnervation of a denervated tongue papilla by a normally nongustatory nerve. Journal of Comparative Neurology 200,
Biologic and Materials Sciences, School of Dentistry, University of Michigan, Ann Arbor, Michigan
THE JOURNAL OF COMPARATIVE NEUROLOGY 409:13 24 (1999) Alterations in Size, Number, and Morphology of Gustatory Papillae and Taste Buds in BDNF Null Mutant Mice Demonstrate Neural Dependence of Developing
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