Faculty of Science and Engineering, School of Engineering, Macquarie University, Sydney, New South Wales 2109, Australia
School of Psychology, Vestibular Research Laboratory, The University of Sydney, Sydney, New South Wales 2050, Australia.
J Neurosci. 2023 Oct 25;43(43):7149-7157. doi: 10.1523/JNEUROSCI.1417-23.2023. Epub 2023 Sep 29.
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. 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.
羊膜动物在内耳前庭器官中进化出了一种独特的突触后末端，称为壶腹，它接收来自 I 型感觉毛细胞的量子和非量子（NQ）突触输入。非量子突触电流包括一个超快成分，据推测该成分是前庭传入神经元对声音和振动产生极高同步指数（向量强度）的基础。在这里，我们提出了三条证据支持以下假说：非量子传递负责两性豚鼠椭圆囊的短潜伏期前庭动作电位的同步。首先，给予 AMPA 受体拮抗剂 CNQX 后，同步前庭神经反应不变，而听觉神经反应完全被阻断。其次，刺激诱发的前庭神经复合动作电位（vCAP）被证明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易释放囊泡的易释放池（RRP）的成对脉冲刺激揭示了豚鼠听觉 cCAP 的前向掩蔽，但前庭 vCAP 完全没有前向掩蔽。结果支持以下结论：毛细胞壶腹突触中非量子传递的快速成分是不知疲倦的，负责瞬态刺激诱发的前庭器官的超快反应。哺乳动物前庭系统驱动神经系统中最快的一些反射途径，确保在陆地上运动时稳定的凝视和姿势控制。为了实现这一点，陆生羊膜动物进化出了一个大型的、独特的壶腹传入末端，它完全包裹着一个或多个前庭毛细胞，这些毛细胞传递由量子和非量子（NQ）突触传递介导的机械感觉信号。我们在豚鼠中提出了几条证据，这些证据表明最敏感的前庭传入非常快，比听觉神经快得多。在这里，我们提出了神经生理学和药理学证据，表明这种前庭速度优势来自 I 型毛细胞到其壶腹伴侣的超快 NQ 电突触传递。
