Abstract:
Amniotes evolved a unique postsynaptic terminal in the inner ear vestibular organs called the calyx that receives both quantal and nonquantal (NQ) synaptic inputs from Type I sensory hair cells. The nonquantal synaptic current includes an ultrafast component that has been hypothesized to underlie the exceptionally high synchronization index (vector strength) of vestibular afferent neurons in response to sound and vibration. Here, we present three lines of evidence supporting the hypothesis that nonquantal transmission is responsible for synchronized vestibular action potentials of short latency in the guinea pig utricle of either sex. First, synchronized vestibular nerve responses are unchanged after administration of the AMPA receptor antagonist CNQX, while auditory nerve responses are completely abolished. Second, stimulus evoked vestibular nerve compound action potentials (vCAP) are shown to occur without measurable synaptic delay and three times shorter than the latency of auditory nerve compound action potentials (cCAP), relative to the generation of extracellular receptor potentials. Third, paired-pulse stimuli designed to deplete the readily releasable pool (RRP) of synaptic vesicles in hair cells reveal forward masking in guinea pig auditory cCAPs, but a complete lack of forward masking in vestibular vCAPs. Results support the conclusion that the fast component of nonquantal transmission at calyceal synapses is indefatigable and responsible for ultrafast responses of vestibular organs evoked by transient stimuli.SIGNIFICANCE STATEMENT The mammalian vestibular system drives some of the fastest reflex pathways in the nervous system, ensuring stable gaze and postural control for locomotion on land. To achieve this, terrestrial amniotes evolved a large, unique calyx afferent terminal which completely envelopes one or more presynaptic vestibular hair cells, which transmits mechanosensory signals mediated by quantal and nonquantal (NQ) synaptic transmission. We present several lines of evidence in the guinea pig which reveals the most sensitive vestibular afferents are remarkably fast, much faster than their auditory nerve counterparts. Here, we present neurophysiological and pharmacological evidence that demonstrates this vestibular speed advantage arises from ultrafast NQ electrical synaptic transmission from Type I hair cells to their calyx partners.
摘要:
羊膜在内耳前庭器官中进化出一种独特的突触后末端,称为花萼,可从I型感觉毛细胞接收定量和非定量突触输入。非定量突触电流包括超快分量,该超快分量被认为是前庭传入神经元响应声音和振动的异常高同步指数(矢量强度)的基础。在这里,我们提供了三条证据,支持以下假设:非定量传递是导致任一性别的豚鼠脑膜中短潜伏期的前庭动作电位同步的原因。首先,给药AMPA受体拮抗剂CNQX后,同步前庭神经反应没有改变,而听神经反应完全废除。第二,刺激诱发的前庭神经复合动作电位(vCAP)显示在没有可测量的突触延迟的情况下发生,并且比听觉神经复合动作电位(cCAP)的潜伏期短三倍,相对于细胞外受体电位的产生。第三,设计用于耗尽毛细胞中容易释放的突触小泡池的成对脉冲刺激显示豚鼠听觉cCAPs的正向掩蔽,但前庭vCAPs完全缺乏前向掩蔽。结果支持这样的结论,即腺突触的非定量传递的快速成分是不知疲倦的,并且是由瞬时刺激引起的前庭器官的超快反应的原因。哺乳动物前庭系统驱动神经系统中一些最快的反射通路,确保在陆地上运动的稳定凝视和姿势控制。为了实现这一点,陆生羊膜进化了一个大的,完全包裹一个或多个突触前前庭毛细胞的独特花萼传入末端,传递由定量和非定量(NQ)突触传递介导的机械感觉信号。我们在豚鼠中提供了几条证据,这些证据表明最敏感的前庭传入神经非常快,比他们的听觉神经要快得多。这里,我们提供了神经生理学和药理学证据,证明前庭速度优势来自于从I型毛细胞到其花萼伴侣的超快NQ电突触传递。