In the developing central nervous system, electrical signaling is thought to rely exclusively on differentiating neurons as they acquire the ability to generate and propagate action potentials. Accordingly, neuroepithelial progenitors (NEPs), which give rise to all neurons and glial cells during development, have been reported to remain electrically passive. Here, we investigated the physiological properties of NEPs at the onset of spontaneous neural activity (SNA) initiating motor behavior in mouse embryonic spinal cord. Using patch-clamp recordings, we discovered that spinal NEPs exhibit spontaneous membrane depolarizations during episodes of SNA. These rhythmic depolarizations exhibited a ventral-to-dorsal gradient with the highest amplitude located in the floor plate, the ventral-most part of the neuroepithelium. Paired recordings revealed that NEPs are coupled via gap junctions and form an electrical syncytium. Although other NEPs were electrically passive, we discovered that floor-plate NEPs generated large Na⁺/Ca²⁺ action potentials. Unlike in neurons, floor-plate action potentials relied primarily on the activation of voltage-gated T-type calcium channels (TTCCs). In situ hybridization showed that all 3 known subtypes of TTCCs are predominantly expressed in the floor plate. During SNA, we found that acetylcholine released by motoneurons rhythmically triggers floor-plate action potentials by acting through nicotinic acetylcholine receptors. Finally, by expressing the genetically encoded calcium indicator GCaMP6f in the floor plate, we demonstrated that neuroepithelial action potentials are associated with calcium waves and propagate along the entire length of the spinal cord. Our work reveals a novel physiological mechanism to generate and propagate electrical signals across a neural structure independently from neurons.

在发育中的中枢神经系统中，电信号被认为完全依赖于分化的神经元，因为它们获得了产生和传播动作电位的能力。因此，据报道，在发育过程中产生所有神经元和神经胶质细胞的神经上皮祖细胞 (NEP) 保持电无源。在这里，我们研究了在小鼠胚胎脊髓中启动运动行为的自发神经活动 (SNA) 开始时 NEP 的生理特性。使用膜片钳记录，我们发现脊髓 NEP 在 SNA 发作期间表现出自发的膜去极化。这些有节奏的去极化表现出腹侧到背侧的梯度，最高振幅位于底板，即神经上皮的最腹侧部分。配对记录显示，NEP 通过间隙连接耦合并形成电合胞体。尽管其他 NEP 是电无源的，但我们发现底板 NEP 会产生大量的 Na⁺ /Ca ²⁺动作电位。与神经元不同，底板动作电位主要依赖于电压门控 T 型钙通道 (TTCC) 的激活。原位杂交显示所有 3 种已知的 TTCC 亚型主要在底板中表达。在 SNA 期间，我们发现运动神经元释放的乙酰胆碱通过烟碱型乙酰胆碱受体有节奏地触发底板动作电位。最后，通过在底板中表达基因编码的钙指示剂 GCaMP6f，我们证明了神经上皮动作电位与钙波相关并沿脊髓的整个长度传播。我们的工作揭示了一种新的生理机制，可以独立于神经元在神经结构中产生和传播电信号。