The floor-plate of His is a non-neuronal electrical conduction pathway

ABSTRACT In the developing central nervous system of vertebrates, the emergence of electrical signals is thought to result exclusively from the differentiation of neurons1–3. Accordingly, the neuro-epithelial progenitors generating neurons and glial cells have been assumed to remain electrically passive. Here, we show that the floor plate of His - a neuro-epithelial organizer located at the ventral midline of the fetal spinal cord4 - has the unexpected ability to generate large biphasic action potentials resulting from the combined activity of voltage-gated T-type calcium channels and sodium channels. Floor plate action potentials are recurrently triggered by the neurotransmitter acetylcholine released from cholinergic motor neurons during early episodes of spontaneous neural activity. Moreover, we found that floor plate cells are connected by gap junctions, form a functional syncytium with other neuro-epithelial progenitor domains and establish a ventral to dorsal depolarization gradient in the neuro-epithelium. Finally, we show that floor plate action potentials are associated with calcium waves and propagate through gap junctions along the length of the fetal spinal cord. Our present work demonstrates that the floor plate of His acts as a unique neuro-epithelial electrical conduction system, sharing functional similarities with the myo-epithelial electrical conduction system of the heart known as the bundle of His5. This discovery profoundly change how we conceive the development, origin, evolution and extent of electrical signals in the central nervous system of vertebrates.