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The Journal of Neuroscience, December 12, 2007, 27(50):13875-13881; doi:10.1523/JNEUROSCI.2517-07.2007

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Behavioral/Systems/Cognitive
Exuberant Neuronal Convergence onto Reduced Taste Bud Targets with Preservation of Neural Specificity in Mice Overexpressing Neurotrophin in the Tongue Epithelium

Faisal N. Zaidi,^1,2,3 Robin F. Krimm,⁵ and Mark C. Whitehead⁴

¹Howard Hughes Medical Institute and Departments of ²Neurobiology, ³Neurosciences, and ⁴Surgery, University of California, San Diego, La Jolla, California 92093, and ⁵Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky 49292

Correspondence should be addressed to Dr. Mark C. Whitehead, Department of Surgery and Anatomy, University of California, San Diego, 9500 Gilman Drive, Mail Code 0604, La Jolla, CA 92093-0604. Email: mcwhitehead{at}ucsd.edu

A mouse fungiform taste bud is innervated by only four to five geniculate ganglion neurons; their peripheral fibers do not branch to other buds. We examined whether the degree or specificity of this exclusive innervation pattern is influenced by brain-derived neurotrophic factor (BDNF), a prominent lingual neurotrophin implicated in taste receptoneural development. Labeled ganglion cells were counted after injecting single buds with different color markers in BDNF-lingual-overexpressing (OE) mice. To evaluate the end-organs, taste buds and a class of putative taste receptor cells were counted from progeny of BDNF-OE mice crossbred with green fluorescent protein (GFP) (gustducin) transgenic mice. Fungiform bud numbers in BDNF-OE mice are 35%, yet geniculate neuron numbers are 195%, of wild-type mice. Neurons labeled by single-bud injections in BDNF-OE animals were increased fourfold versus controls. Injecting three buds, each with different color markers, resulted in predominantly single-labeled ganglion cells, a discrete innervation pattern similar to controls. Thus, hyper-innervation of BDNF-OE buds involves many neurons innervating single buds, not increased fiber branching. Therefore, both wild-type and BDNF-OE mice exhibit, in fungiform buds, the same, "discrete" receptoneural pattern, this despite dramatic neurotrophin overexpression-related decreases in bud numbers and increases in innervation density. Hyperinnervation did not affect GFP positive cell numbers; proportions of GFP cells in BDNF-OE buds were the same as in wild-type mice. Total numbers of ganglion cells innervating buds in transgenic mice are similar to controls; the density of taste input to the brain appears maintained despite dramatically reduced receptor organs and increased ganglion cells.

Key words: taste bud; geniculate; ganglion; innervation; mouse; neurotrophin

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Received June 4, 2007; revised Oct. 18, 2007; accepted Oct. 28, 2007.

Correspondence should be addressed to Dr. Mark C. Whitehead, Department of Surgery and Anatomy, University of California, San Diego, 9500 Gilman Drive, Mail Code 0604, La Jolla, CA 92093-0604. Email: mcwhitehead{at}ucsd.edu

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