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Vertebrate taste-bud development: are salamanders the model?
LETTERS striatum ‘plays a role’ in response gating of prey-catching via pretectum, I hope the reader will not get the impression that this is the only connection mediating striatotectal influences (we have found a direct connection in salamanders8). The important point – based on neuroanatomical, neurophysiological and behavioral data – is that prey-catching in anurans can take advantage of a modulatory striato–pretecto–tectal channel in order to translate
perception into action, a channel which, in mammals, obviously does not exist. Jörg-Peter Ewert Neurobiologie, Fachbereich Biologie/Chemie, Universität Kassel, 34132 Kassel, Bundesrepublik, Germany. References 1 Gonzalez, A. and Smeets, W.J.A.J. (1991) J. Comp. Neurol. 303, 457–477
Vertebrate taste-bud development: are salamanders the model? Some decades ago, Stone and associates reported that newt taste buds would develop in the absence of gustatory innervation1 and could subsequently survive in the absence of any innervation2. More recently Northcutt and Barlow3 examined axolotl taste-bud development and, with embryonic transplantation and dye injection, confirmed and extended these classic observations. Rather than migrating in from either the neural crest or placodes, axolotl taste-cell precursors originate in local epithelial tissue where their progeny can differentiate into taste buds even in the absence of innervation. Does the well-established nerve-independence of salamander taste buds also apply to mammalian taste buds, as Northcutt and Barlow now propose? More than 90% of rat or mouse vallate taste buds develop postnatally, provided that the vallate papilla remains innervated4–6. If, instead, the IXth nerve is interrupted in the newborn rat tongue (P0–P3), it both prevents the development of most vallate taste buds7,8 and also permanently eliminates the competence of the reinnervated gustatory epithelium to support taste bud development9,10. I here summarize recent evidence establishing that prenatal taste bud development is also nerve-dependent in mammals. The embryonic absence of brainderived neurotrophic factor (BDNF) in bdnf-null mutant mice caused a loss of gustatory innervation associated with the severely impaired development of taste papillae and taste buds11–13. Specifically, the sparseness of gustatory innervation was highly correlated with a smaller gustatory epithelium (r ⫽ ⫹0.94) and fewer taste buds (r ⫽ ⫹0.96) (Ref. 13). The rescue of small numbers of BDNF-deprived taste neurons by local epithelial factors, such as NT-3, accounts for the residual presence of a few vallate taste buds5,13. Using a quite different method to destroy developing tongue sensory neurons, Morris-Wiman et al. almost completely prevented the development of fungiform papillae and
their taste buds in normal mouse embryos injected with the neurotoxin, beta-bungarotoxin14. By eliminating most of the gustatory innervation, null mutations of bdnf or trkB also eliminated many fungiform papillae and taste buds12,13,15,16. Those fungiform taste buds that remained were likely to have obtained support from the rich plexus of trigeminal nerve fibers present in each fungiform papilla. Trigeminal axons can provide modest trophic support of adult taste buds17. In contrast to the partial persistence of scattered fungiform taste buds and papillae after nerve transection in adult rats, chorda-lingual nerve transection in neonates caused every fungiform papilla to lose its taste bud and revert to a filiform or filiform-like spine18. This observation decisively establishes that, like vallate taste buds, fungiform taste buds are also wholly nerve-dependent at birth. The unanimity of recent studies on the effects of sensory denervation on fetal and newborn rodent tongues has reconfirmed the canonical view that mammalian tastebud development is nerve-dependent. More precisely, mammalian taste axons appear to contribute sequentially to papilla morphogenesis, gustatory competence, and taste-bud formation. Comparative biologists may note with satisfaction that the singularity of taste-bud development in salamanders presents a splendid opportunity to examine epithelial cell interactions uncomplicated by the reality of the nerve dependence of taste bud development in mammals. Bruce Oakley Dept of Biology, University of Michigan, Ann Arbor, MI 48l09, USA. References 1 Stone, L.S. (1940) J. Exp. Zool. 83, 481–506 2 Wright, M.R. (1964) J. Exp. Zool. 156, 377–390 3 Northcutt, R.G. and Barlow, L.A. (1998) Trends Neurosci. 21, 38–42
TO THE EDITOR
2 Wilczynski, W. and Northcutt, R.G. (1983) J. Comp. Neurol. 214, 333–343 3 Marín, O. et al. (1997) J. Comp. Neurol. 380, 23–50 4 Marín, O. et al. (1997) J. Comp. Neurol. 378, 50–69 5 Glagow, M. and Ewert, J-P. (1996) Neurosci. Lett. 220, 215–218 6 Glagow, M. and Ewert, J-P. (1997) J. Comp. Physiol. 180, 1–9 7 Glagow, M. and Ewert, J-P. (1997) J. Comp. Physiol. 180, 11–18 8 Finkenstädt, T. et al. (1983) Cell Tissue Res. 234, 39–55
4 Hosley, M.A. and Oakley, B. (1987) Anat. Rec. 218, 216–222 5 Cooper, D. and Oakley, B. (1998) Dev. Brain Res. 105, 79–84 6 Oakley, B. et al. (1991) Dev. Brain Res. 58, 215–221 7 Hosley, M.A. et al. (1987) J. Comp. Neurol. 260, 224–232 8 Hosley, M.A. et al. (1987) J. Neurosci. 7, 2075–2080 9 Oakley, B. (1993) Dev. Brain Res. 72, 259–264 10 Oakley, B. (1993) in Mechanisms of Taste Transduction (Simon, S.A. and Roper, S.D., eds), pp. 105–125, CRC Press 11 Zhang, C. et al. (1997) NeuroReport 8, 1013–1017 12 Nosrat, C. et al. (1997) Development 124, 1335–1342 13 Oakley, B. et al. (1998) Dev. Brain Res. 105, 85–96 14 Morris-Wiman, J. et al. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 15 Fritzsch, B. et al. (1997) Int. J. Dev. Neurosci. 15, 563–576 16 Oakley, B. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 17 Oakley, B. et al. (1990) Neuroscience 36, 831–838 18 Nagato, T. et al. (1995) Acta Anat. 153, 301–309
There is no longer much doubt that in vertebrates a regional specification of endoderm does occur during gastrulation1, or even before2, and, as Northcutt and Barlow3 have shown, a population of tastebud progenitor cells might be established at that time. However, comparative anatomical observations on fish taste buds caution us not to be too hasty in extending the scenario, proposed initially for amphibians, to vertebrates generally. Firstly, taste buds in fishes are not confined to regions of the pharyngeal endoderm that involute during gastrulation, but (indistinguishable in ultrastructure from those of the mouth cavity4), can occur on barbels and even the tips of pectoral-fin rays as well. Secondly, the number of innervated taste buds could depend on specific signals arriving from taste buds or their progenitors in amphibia. However, at least in fishes, early and repeated taste-bud stimulation (i.e. use), might be important, not only in maintaining taste-bud innervation, but could also lead to a multiplication of innervated taste-bud sites in the growing TINS Vol. 21, No. 8, 1998
337
LETTERS
TO THE EDITOR animal. This scenario, which differs from the old ‘induction model’ and ought to be seen as an extension of the model suggested by Northcutt and Barlow3, could be one of the reasons why a fish species, such as trout, that experiences frequent and varied stimulation of taste buds through a wide range of food items possesses much higher taste-bud densities than a deep-sea
fish, that is, a species that lives in an environment characterized by lack of food and food variety5.
Reply
Cultured embryonic rodent tongues devoid of innervation do not survive until taste buds normally form, and these experiments have therefore not resolved this issue14,15. Results from BDNF and trkB knockout mice are equivocal because examination of these mice has been generally restricted to postnatal stages after the first taste buds have differentiated16–19. However, in mice examined when taste buds first develop20, the number of taste buds in control and trkB-knockout mice was comparable, although taste buds of knockout mice lacked normal innervation. As development progressed, trkB-null mice gradually lost taste buds so that taste-bud number was drastically reduced postnatally, consistent with a neural maintenance paradigm, and with the results of other researchers16–19. We have argued that taste-bud differentiation initially is nerve-independent, but that once taste buds differentiate, they become reliant on nerves for maintenance21,22. Future experimental approaches should take into account these two phases of taste-bud development. Dr Meyer-Rochow’s point about external taste buds found in fish is also well taken. Nonetheless, many fishes only have oropharyngeal taste buds, and therefore the model we propose could readily apply. However, the embryonic origin of external taste buds found in some fishes, and the manner in which they arise during embryogenesis are intriguing issues. When present in fish, external taste buds reside in skin which is derived from ectoderm. Thus, if these buds arise locally, as do those of mammals23 and amphibians24, they would be ectodermal in origin. Interestingly, in mammals and amphibians, where taste buds are exclusively oropharyngeal, taste buds arise from both ectoderm and endoderm. In mammals, taste buds in the mouth arise predominantly from ectoderm23, whereas those in the pharynx arise from endoderm25. Although most taste buds in salamanders arise from endoderm24, those located most anteriorly arise from ectoderm26. Thus, taste buds can arise from either germ layer. This developmental plasticity might have allowed the appearance during evolution of external, ectodermal taste buds in some groups of fishes via conserved developmental mechanisms. However, until taste-
Dr Oakley makes the point that differentiated taste buds are largely nerve-dependent in mammals. However, the nerve-dependence of differentiated taste buds is distinct from the role nerves might play embryonically in the initial formation of taste buds. During embryogenesis, taste buds differentiate from a population of putatively equivalent epithelial cells within the mouth and pharynx. We have investigated whether taste buds are induced in this epithelium by contact with ingrowing nerves. Induction is defined as the receipt of a signal from one set of cells that changes the fate of the recipient cells; in the absence of inductive signals from nerves, taste buds therefore should not form. In amphibians, we have tested this hypothesis explicitly, and rejected it1,2. Although amphibian taste buds differentiate3 or survive to some degree4–7 without cranial-nerve contact, we have shown that taste buds form in the total absence of innervation1,2. The comparable experiment has not been performed in any mammal, and thus the question of differences in the embryogenesis of taste buds in mammals versus amphibians remains unanswered. All tests so far of the role of nerves in the development of mammalian taste buds have used postnatal rodents8–10. At birth, however, incipient taste buds are already present in the lingual epithelium and are innervated11–14. Cutting nerves postnatally8–10 therefore sheds little light on inductive events that produce taste buds embryonically. Instead, the loss of taste buds after denervation demonstrates that differentiated taste buds are maintained by nerves. To test whether mammalian taste buds are induced by nerves, gustatory nerves must be prevented completely from reaching the epithelium where taste buds will reside, and the nerve-naive epithelium examined at birth, when taste buds first appear. If taste buds fail to form under these conditions, then we will be able to make a clear distinction between how mammals and amphibians generate taste buds (that is, mammalian taste buds are induced by nerves whereas those of amphibians are not). However, until this type of experiment has been performed, amphibian and mammalian studies cannot be compared directly. 338
TINS Vol. 21, No. 8, 1998
V.B. Meyer-Rochow Dept of Biology, University of Oulu, SF-90570 Oulu, Finland.
References 1 Bouwmeester, T. et al. (1996) Nature 382, 595–601 2 Henry, G.I. (1996) Development 122, 225–232 3 Northcutt, R.G. and Barlow L.A. (1998) Trends Neurosci. 21, 38–43 4 Ovalle, W.K. and Shinn, S.L. (1977) Cell Tissue Res. 178, 378–384 5 Meyer-Rochow, V.B. (1981) Zool. J. Linn. Soc. 71, 413–426
bud development in fishes is attacked experimentally, the question of differences between the development of external and internal taste buds remains one of pure conjecture. Linda A. Barlow Dept of Biological Sciences, University of Denver, Denver, CO 80208, USA.
R. Glenn Northcutt Dept of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, CA 92093, USA. References 1 Barlow, L.A. and Northcutt, R.G. (1997) Development 124, 949–957 2 Barlow, L.A. et al. (1996) Development 122, 1103–1111 3 Stone, L.S. (1940) J. Exp. Zool. 83, 481–506 4 Wright, M.R. (1964) J. Exp. Zool. 156, 377–390 5 Poritsky, R. and Singer, M. (1963) J. Exp. Zool. 153, 211–218 6 Poritsky, R. and Singer, M. (1977) Anat. Rec. 188, 219–228 7 Robbins, N. (1967) Exp. Neurol. 17, 364–380 8 Hosley, M.A. et al. (1987) J. Comp. Neurol. 260, 224–232 9 Hosley, M.A. et al. (1987) J. Neurosci. 7, 2075–2080 10 Oakley, B. (1993) Dev. Brain Res. 72, 259–264 11 Oakley, B. et al. (1991) Dev. Brain Res. 58, 215–221 12 Oakley, B. (1993) in Mechanisms of Taste Transduction (Simon, S.A. and Roper, S.D., eds), pp. 105–125, CRC Press 13 Hosley, M.A. and Oakley, B. (1987) Anat. Rec. 218, 216–222 14 Farbman, A.I. and Mbiene, J-P. (1991) J. Comp. Neurol. 304, 172–186 15 Mbiene, J-P. et al. (1997) J. Comp. Neurol. 377, 324–340 16 Nosrat, C.A. et al. 1997 Development 124, 1333–1342 17 Zhang, C.X. et al. (1997) NeuroReport 8, 1013–1017 18 Oakley, B. et al. (1998) Dev. Brain Res. 105, 85–96 19 Cooper, D. and Oakley, B. (1998) Dev. Brain Res. 105, 79–84 20 Fritzsch, B. et al. (1997) Int. J. Dev. Neurosci. 15, 563–576 21 Barlow, L.A. and Northcutt, R.G. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 22 Northcutt, R.G. and Barlow, L.A. (1998) Trends Neurosci. 21, 38–42 23 Stone, L.M. et al. (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 1916–1920 24 Barlow, L.A. and Northcutt, R.G. (1995) Dev. Biol. 169, 273–285 25 Stone, L.M. et al. (1995) Chem. Senses 20, 785–786 26 Barlow, L.A. Chem. Senses (in press)
perception into action, a channel which, in mammals, obviously does not exist. Jörg-Peter Ewert Neurobiologie, Fachbereich Biologie/Chemie, Universität Kassel, 34132 Kassel, Bundesrepublik, Germany. References 1 Gonzalez, A. and Smeets, W.J.A.J. (1991) J. Comp. Neurol. 303, 457–477
Vertebrate taste-bud development: are salamanders the model? Some decades ago, Stone and associates reported that newt taste buds would develop in the absence of gustatory innervation1 and could subsequently survive in the absence of any innervation2. More recently Northcutt and Barlow3 examined axolotl taste-bud development and, with embryonic transplantation and dye injection, confirmed and extended these classic observations. Rather than migrating in from either the neural crest or placodes, axolotl taste-cell precursors originate in local epithelial tissue where their progeny can differentiate into taste buds even in the absence of innervation. Does the well-established nerve-independence of salamander taste buds also apply to mammalian taste buds, as Northcutt and Barlow now propose? More than 90% of rat or mouse vallate taste buds develop postnatally, provided that the vallate papilla remains innervated4–6. If, instead, the IXth nerve is interrupted in the newborn rat tongue (P0–P3), it both prevents the development of most vallate taste buds7,8 and also permanently eliminates the competence of the reinnervated gustatory epithelium to support taste bud development9,10. I here summarize recent evidence establishing that prenatal taste bud development is also nerve-dependent in mammals. The embryonic absence of brainderived neurotrophic factor (BDNF) in bdnf-null mutant mice caused a loss of gustatory innervation associated with the severely impaired development of taste papillae and taste buds11–13. Specifically, the sparseness of gustatory innervation was highly correlated with a smaller gustatory epithelium (r ⫽ ⫹0.94) and fewer taste buds (r ⫽ ⫹0.96) (Ref. 13). The rescue of small numbers of BDNF-deprived taste neurons by local epithelial factors, such as NT-3, accounts for the residual presence of a few vallate taste buds5,13. Using a quite different method to destroy developing tongue sensory neurons, Morris-Wiman et al. almost completely prevented the development of fungiform papillae and
their taste buds in normal mouse embryos injected with the neurotoxin, beta-bungarotoxin14. By eliminating most of the gustatory innervation, null mutations of bdnf or trkB also eliminated many fungiform papillae and taste buds12,13,15,16. Those fungiform taste buds that remained were likely to have obtained support from the rich plexus of trigeminal nerve fibers present in each fungiform papilla. Trigeminal axons can provide modest trophic support of adult taste buds17. In contrast to the partial persistence of scattered fungiform taste buds and papillae after nerve transection in adult rats, chorda-lingual nerve transection in neonates caused every fungiform papilla to lose its taste bud and revert to a filiform or filiform-like spine18. This observation decisively establishes that, like vallate taste buds, fungiform taste buds are also wholly nerve-dependent at birth. The unanimity of recent studies on the effects of sensory denervation on fetal and newborn rodent tongues has reconfirmed the canonical view that mammalian tastebud development is nerve-dependent. More precisely, mammalian taste axons appear to contribute sequentially to papilla morphogenesis, gustatory competence, and taste-bud formation. Comparative biologists may note with satisfaction that the singularity of taste-bud development in salamanders presents a splendid opportunity to examine epithelial cell interactions uncomplicated by the reality of the nerve dependence of taste bud development in mammals. Bruce Oakley Dept of Biology, University of Michigan, Ann Arbor, MI 48l09, USA. References 1 Stone, L.S. (1940) J. Exp. Zool. 83, 481–506 2 Wright, M.R. (1964) J. Exp. Zool. 156, 377–390 3 Northcutt, R.G. and Barlow, L.A. (1998) Trends Neurosci. 21, 38–42
TO THE EDITOR
2 Wilczynski, W. and Northcutt, R.G. (1983) J. Comp. Neurol. 214, 333–343 3 Marín, O. et al. (1997) J. Comp. Neurol. 380, 23–50 4 Marín, O. et al. (1997) J. Comp. Neurol. 378, 50–69 5 Glagow, M. and Ewert, J-P. (1996) Neurosci. Lett. 220, 215–218 6 Glagow, M. and Ewert, J-P. (1997) J. Comp. Physiol. 180, 1–9 7 Glagow, M. and Ewert, J-P. (1997) J. Comp. Physiol. 180, 11–18 8 Finkenstädt, T. et al. (1983) Cell Tissue Res. 234, 39–55
4 Hosley, M.A. and Oakley, B. (1987) Anat. Rec. 218, 216–222 5 Cooper, D. and Oakley, B. (1998) Dev. Brain Res. 105, 79–84 6 Oakley, B. et al. (1991) Dev. Brain Res. 58, 215–221 7 Hosley, M.A. et al. (1987) J. Comp. Neurol. 260, 224–232 8 Hosley, M.A. et al. (1987) J. Neurosci. 7, 2075–2080 9 Oakley, B. (1993) Dev. Brain Res. 72, 259–264 10 Oakley, B. (1993) in Mechanisms of Taste Transduction (Simon, S.A. and Roper, S.D., eds), pp. 105–125, CRC Press 11 Zhang, C. et al. (1997) NeuroReport 8, 1013–1017 12 Nosrat, C. et al. (1997) Development 124, 1335–1342 13 Oakley, B. et al. (1998) Dev. Brain Res. 105, 85–96 14 Morris-Wiman, J. et al. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 15 Fritzsch, B. et al. (1997) Int. J. Dev. Neurosci. 15, 563–576 16 Oakley, B. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 17 Oakley, B. et al. (1990) Neuroscience 36, 831–838 18 Nagato, T. et al. (1995) Acta Anat. 153, 301–309
There is no longer much doubt that in vertebrates a regional specification of endoderm does occur during gastrulation1, or even before2, and, as Northcutt and Barlow3 have shown, a population of tastebud progenitor cells might be established at that time. However, comparative anatomical observations on fish taste buds caution us not to be too hasty in extending the scenario, proposed initially for amphibians, to vertebrates generally. Firstly, taste buds in fishes are not confined to regions of the pharyngeal endoderm that involute during gastrulation, but (indistinguishable in ultrastructure from those of the mouth cavity4), can occur on barbels and even the tips of pectoral-fin rays as well. Secondly, the number of innervated taste buds could depend on specific signals arriving from taste buds or their progenitors in amphibia. However, at least in fishes, early and repeated taste-bud stimulation (i.e. use), might be important, not only in maintaining taste-bud innervation, but could also lead to a multiplication of innervated taste-bud sites in the growing TINS Vol. 21, No. 8, 1998
337
LETTERS
TO THE EDITOR animal. This scenario, which differs from the old ‘induction model’ and ought to be seen as an extension of the model suggested by Northcutt and Barlow3, could be one of the reasons why a fish species, such as trout, that experiences frequent and varied stimulation of taste buds through a wide range of food items possesses much higher taste-bud densities than a deep-sea
fish, that is, a species that lives in an environment characterized by lack of food and food variety5.
Reply
Cultured embryonic rodent tongues devoid of innervation do not survive until taste buds normally form, and these experiments have therefore not resolved this issue14,15. Results from BDNF and trkB knockout mice are equivocal because examination of these mice has been generally restricted to postnatal stages after the first taste buds have differentiated16–19. However, in mice examined when taste buds first develop20, the number of taste buds in control and trkB-knockout mice was comparable, although taste buds of knockout mice lacked normal innervation. As development progressed, trkB-null mice gradually lost taste buds so that taste-bud number was drastically reduced postnatally, consistent with a neural maintenance paradigm, and with the results of other researchers16–19. We have argued that taste-bud differentiation initially is nerve-independent, but that once taste buds differentiate, they become reliant on nerves for maintenance21,22. Future experimental approaches should take into account these two phases of taste-bud development. Dr Meyer-Rochow’s point about external taste buds found in fish is also well taken. Nonetheless, many fishes only have oropharyngeal taste buds, and therefore the model we propose could readily apply. However, the embryonic origin of external taste buds found in some fishes, and the manner in which they arise during embryogenesis are intriguing issues. When present in fish, external taste buds reside in skin which is derived from ectoderm. Thus, if these buds arise locally, as do those of mammals23 and amphibians24, they would be ectodermal in origin. Interestingly, in mammals and amphibians, where taste buds are exclusively oropharyngeal, taste buds arise from both ectoderm and endoderm. In mammals, taste buds in the mouth arise predominantly from ectoderm23, whereas those in the pharynx arise from endoderm25. Although most taste buds in salamanders arise from endoderm24, those located most anteriorly arise from ectoderm26. Thus, taste buds can arise from either germ layer. This developmental plasticity might have allowed the appearance during evolution of external, ectodermal taste buds in some groups of fishes via conserved developmental mechanisms. However, until taste-
Dr Oakley makes the point that differentiated taste buds are largely nerve-dependent in mammals. However, the nerve-dependence of differentiated taste buds is distinct from the role nerves might play embryonically in the initial formation of taste buds. During embryogenesis, taste buds differentiate from a population of putatively equivalent epithelial cells within the mouth and pharynx. We have investigated whether taste buds are induced in this epithelium by contact with ingrowing nerves. Induction is defined as the receipt of a signal from one set of cells that changes the fate of the recipient cells; in the absence of inductive signals from nerves, taste buds therefore should not form. In amphibians, we have tested this hypothesis explicitly, and rejected it1,2. Although amphibian taste buds differentiate3 or survive to some degree4–7 without cranial-nerve contact, we have shown that taste buds form in the total absence of innervation1,2. The comparable experiment has not been performed in any mammal, and thus the question of differences in the embryogenesis of taste buds in mammals versus amphibians remains unanswered. All tests so far of the role of nerves in the development of mammalian taste buds have used postnatal rodents8–10. At birth, however, incipient taste buds are already present in the lingual epithelium and are innervated11–14. Cutting nerves postnatally8–10 therefore sheds little light on inductive events that produce taste buds embryonically. Instead, the loss of taste buds after denervation demonstrates that differentiated taste buds are maintained by nerves. To test whether mammalian taste buds are induced by nerves, gustatory nerves must be prevented completely from reaching the epithelium where taste buds will reside, and the nerve-naive epithelium examined at birth, when taste buds first appear. If taste buds fail to form under these conditions, then we will be able to make a clear distinction between how mammals and amphibians generate taste buds (that is, mammalian taste buds are induced by nerves whereas those of amphibians are not). However, until this type of experiment has been performed, amphibian and mammalian studies cannot be compared directly. 338
TINS Vol. 21, No. 8, 1998
V.B. Meyer-Rochow Dept of Biology, University of Oulu, SF-90570 Oulu, Finland.
References 1 Bouwmeester, T. et al. (1996) Nature 382, 595–601 2 Henry, G.I. (1996) Development 122, 225–232 3 Northcutt, R.G. and Barlow L.A. (1998) Trends Neurosci. 21, 38–43 4 Ovalle, W.K. and Shinn, S.L. (1977) Cell Tissue Res. 178, 378–384 5 Meyer-Rochow, V.B. (1981) Zool. J. Linn. Soc. 71, 413–426
bud development in fishes is attacked experimentally, the question of differences between the development of external and internal taste buds remains one of pure conjecture. Linda A. Barlow Dept of Biological Sciences, University of Denver, Denver, CO 80208, USA.
R. Glenn Northcutt Dept of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, CA 92093, USA. References 1 Barlow, L.A. and Northcutt, R.G. (1997) Development 124, 949–957 2 Barlow, L.A. et al. (1996) Development 122, 1103–1111 3 Stone, L.S. (1940) J. Exp. Zool. 83, 481–506 4 Wright, M.R. (1964) J. Exp. Zool. 156, 377–390 5 Poritsky, R. and Singer, M. (1963) J. Exp. Zool. 153, 211–218 6 Poritsky, R. and Singer, M. (1977) Anat. Rec. 188, 219–228 7 Robbins, N. (1967) Exp. Neurol. 17, 364–380 8 Hosley, M.A. et al. (1987) J. Comp. Neurol. 260, 224–232 9 Hosley, M.A. et al. (1987) J. Neurosci. 7, 2075–2080 10 Oakley, B. (1993) Dev. Brain Res. 72, 259–264 11 Oakley, B. et al. (1991) Dev. Brain Res. 58, 215–221 12 Oakley, B. (1993) in Mechanisms of Taste Transduction (Simon, S.A. and Roper, S.D., eds), pp. 105–125, CRC Press 13 Hosley, M.A. and Oakley, B. (1987) Anat. Rec. 218, 216–222 14 Farbman, A.I. and Mbiene, J-P. (1991) J. Comp. Neurol. 304, 172–186 15 Mbiene, J-P. et al. (1997) J. Comp. Neurol. 377, 324–340 16 Nosrat, C.A. et al. 1997 Development 124, 1333–1342 17 Zhang, C.X. et al. (1997) NeuroReport 8, 1013–1017 18 Oakley, B. et al. (1998) Dev. Brain Res. 105, 85–96 19 Cooper, D. and Oakley, B. (1998) Dev. Brain Res. 105, 79–84 20 Fritzsch, B. et al. (1997) Int. J. Dev. Neurosci. 15, 563–576 21 Barlow, L.A. and Northcutt, R.G. in XII Int. Symp. Olf. and Taste, Ann. New York Acad. Sci. (in press) 22 Northcutt, R.G. and Barlow, L.A. (1998) Trends Neurosci. 21, 38–42 23 Stone, L.M. et al. (1995) Proc. Natl. Acad. Sci. U. S. A. 92, 1916–1920 24 Barlow, L.A. and Northcutt, R.G. (1995) Dev. Biol. 169, 273–285 25 Stone, L.M. et al. (1995) Chem. Senses 20, 785–786 26 Barlow, L.A. Chem. Senses (in press)