Skyberg Rolf, Sun Chengsan, Hill David L
Department of Psychology, University of Virginia, Charlottesville, Virginia 22904-4400.
Department of Psychology, University of Virginia, Charlottesville, Virginia 22904-4400
J Neurosci. 2017 Aug 9;37(32):7619-7630. doi: 10.1523/JNEUROSCI.3838-16.2017. Epub 2017 Jul 4.
Neural activity plays a critical role in the development of central circuits in sensory systems. However, the maintenance of these circuits at adulthood is usually not dependent on sensory-elicited neural activity. Recent work in the mouse gustatory system showed that selectively deleting the primary transduction channel for sodium taste, the epithelial sodium channel (ENaC), throughout development dramatically impacted the organization of the central terminal fields of three nerves that carry taste information to the nucleus of the solitary tract. More specifically, deleting ENaCs during development prevented the normal maturation of the fields. The present study was designed to extend these findings by testing the hypothesis that the loss of sodium taste activity impacts the maintenance of the normal adult terminal field organization in male and female mice. To do this, we used an inducible Cre-dependent genetic recombination strategy to delete ENaC function after terminal field maturation occurred. We found that removal of sodium taste neural activity at adulthood resulted in significant reorganization of mature gustatory afferent terminal fields in the nucleus of the solitary tract. Specifically, the chorda tympani and greater superficial petrosal nerve terminal fields were 1.4× and 1.6× larger than age-matched controls, respectively. By contrast, the glossopharyngeal nerve, which is not highly sensitive to sodium taste stimulation, did not undergo terminal field reorganization. These surprising results suggest that gustatory nerve terminal fields remain plastic well into adulthood, which likely impacts central coding of taste information and taste-related behaviors with altered taste experience. Neural activity plays a major role in the development of sensory circuits in the mammalian brain. However, the importance of sensory-driven activity in maintaining these circuits at adulthood, especially in subcortical structures, appears to be much less. Here, we tested whether the loss of sodium taste activity in adult mice impacts the maintenance of how taste nerves project to the first central relay. We found that specific loss of sodium-elicited taste activity at adulthood produced dramatic and selective reorganization of terminal fields in the brainstem. This demonstrates, for the first time, that taste-elicited activity is necessary for the normal maintenance of central gustatory circuits at adulthood and highlights a level of plasticity not seen in other sensory system subcortical circuits.
神经活动在感觉系统中枢回路的发育中起着关键作用。然而，这些回路在成年期的维持通常不依赖于感觉诱发的神经活动。最近在小鼠味觉系统中的研究表明，在整个发育过程中选择性删除钠味觉的主要转导通道——上皮钠通道（ENaC），会显著影响将味觉信息传递到孤束核的三条神经的中枢终末场的组织。更具体地说，在发育过程中删除ENaC会阻止这些终末场的正常成熟。本研究旨在通过检验钠味觉活动丧失会影响成年雄性和雌性小鼠正常成年终末场组织维持这一假设来扩展这些发现。为此，我们使用了一种诱导型Cre依赖性基因重组策略，在终末场成熟后删除ENaC功能。我们发现成年期去除钠味觉神经活动会导致孤束核中成熟味觉传入终末场的显著重组。具体而言，鼓索神经和岩大浅神经终末场分别比年龄匹配的对照组大1.4倍和1.6倍。相比之下，对钠味觉刺激不太敏感的舌咽神经没有发生终末场重组。这些惊人的结果表明，味觉神经终末场在成年后很长时间内仍具有可塑性，这可能会影响味觉信息的中枢编码以及与味觉体验改变相关的味觉行为。神经活动在哺乳动物大脑感觉回路的发育中起主要作用。然而，感觉驱动的活动在成年期维持这些回路，尤其是在皮层下结构中的重要性似乎要小得多。在这里，我们测试了成年小鼠钠味觉活动的丧失是否会影响味觉神经投射到第一个中枢中继站的维持方式。我们发现成年期钠诱发的味觉活动的特异性丧失会导致脑干终末场的显著且选择性重组。这首次证明，味觉诱发的活动对于成年期中枢味觉回路的正常维持是必要的，并突出了一种在其他感觉系统皮层下回路中未见的可塑性水平。
