The ring of glutamates at the intracellular end of the pore of muscle nicotinic acetylcholine receptors (AChR) is, by far, the ring of pore-lining ionizable side chains that lowers the energetic cost of cation conduction the most. Although these glutamates have received much attention, many of their properties have remained unexplained, especially when compared to the properties of similar rings in voltage-dependent Ca2+ channels and cyclic-nucleotide gated channels. In my talk, I will present new insight into the properties of this ring of AChR glutamates obtained from single-channel electrophysiological recordings. Our results indicate: that all four wild-type glutamate side chains in the ring (the fifth residue being a glutamine) are fully deprotonated in the 6.0'9.0 pH range; that only two of them contribute to the size of the single-channel current; that these side chains must be able to adopt alternate conformations that either allow or prevent their negative charges from increasing the rate of cation conduction; and that the location of these glutamate side chains in the ambivalent membrane'water interface is critical for their largely unshifted pKa values and for the unexpected impact of their conformational dynamics on cation permeation.