Maintenance of Mouse Gustatory Terminal Field Organization Is Dependent on BDNF at Adulthood

The rodent peripheral gustatory system is especially plastic during early postnatal development and maintains significant anatomical plasticity into adulthood. Thus, taste information carried from the tongue to the brain is built and maintained on a background of anatomical circuits that have the capacity to change throughout the animal's lifespan. Recently, the neurotrophin brain-derived neurotrophic factor (BDNF) was shown to be required in the tongue to maintain normal levels of innervation in taste buds at adulthood, indicating that BDNF is a key molecule in the maintenance of nerve/target matching in taste buds. Here, we tested whether maintenance of the central process of these gustatory nerves at adulthood also relies on BDNF by using male and female transgenic mice with inducible CreERT2 under the control of the keratin 14 promoter or under control of the ubiquitin promoter to remove Bdnf from the tongue or from all tissues, respectively. We found that the terminal fields of gustatory nerves in the nucleus of the solitary tract were expanded when Bdnf was removed from the tongue at adulthood and with even larger and more widespread changes in mice where Bdnf was removed from all tissues. Removal of Bdnf did not affect numbers of ganglion cells that made up the nerves and did not affect peripheral, whole-nerve taste responses. We conclude that normal expression of Bdnf in gustatory structures is required to maintain normal levels of innervation at adulthood and that the central effects of Bdnf removal are opposite of those in the tongue.

SIGNIFICANCE STATEMENT BDNF plays a major role in the development and maintenance of proper innervation of taste buds. However, the importance of BDNF in maintaining innervation patterns of gustatory nerves into central targets has not been assessed. Here, we tested whether Bdnf removal from the tongue or from all structures in adult mice impacts the maintenance of how taste nerves project to the first central relay. Deletion of Bdnf from the tongue and from all tissues led to a progressively greater expansion of terminal fields. This demonstrates, for the first time, that BDNF is necessary for the normal maintenance of central gustatory circuits at adulthood and further highlights a level of plasticity not seen in other sensory system subcortical circuits.