Size-related properties of vestibular afferent fibers in the frog: differential synaptic activation of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors.

Vestibular afferent fibers exhibit a specific, cell size-related uptake of aspartate and glycine [Straka H. et al. (1995) Neuroscience 70, 685-696]. A similar, size-related coexistence of glycine and glutamate had been reported earlier for these fibers [Reichenberger I. and Dieringer N. (1994) J. comp. Neurol. 349, 603-614]. Taken together, these results suggest a size-related co-release of both amino acids and the activation of different glutamate receptors in second order vestibular neurons. To test this hypothesis we stimulated the VIIIth nerve and recorded the responses of central vestibular neurons in the isolated brainstem of frogs before and during the application of the N-methyl-D-aspartate antagonists (7-chlorokynurenic acid and D-(-)-2-amino-5-phosphonovaleric acid). The presence of either one of these antagonists provoked a dose-dependent and Mg(2+)-sensitive partial block of the monosynaptic responses recorded extra- or intracellularly. This implies that afferent-evoked responses in central vestibular neurons are composed of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor-mediated components. In most of the intracellularly recorded neurons (21 out of 24) the relative amplitude of the N-methyl-D-aspartate receptor-mediated component decreased with an increase in stimulus intensity. Since electric stimulation recruits thick afferents at a lower current intensity than thin afferent fibers, our results imply a co-activation of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors by thick vestibular afferents. At a given stimulus intensity the amplitude of the N-methyl-D-aspartate receptor-mediated component differed between neurons. The results of this study extend the list of known anatomical, histochemical and physiological properties that distinguish thick from thinner vestibular afferent fibers. In spite of this detailed knowledge, however, the physiological role of thick vestibular afferents is so far unclear. The novel concept of a size-related co-activation of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors by vestibular afferent fibers establishes the basis for more specific physiological hypotheses.