Canal-specific excitation and inhibition of frog second-order vestibular neurons

Second-order vestibular neurons (secondary VNs) were identified in the in vitro frog brain by their monosynaptic excitation following electrical stimulation of the ipsilateral VIIIth nerve. Ipsilateral disynaptic inhibitory postsynaptic potentials were revealed by bath application of the glycine antagonist strychnine or of the gamma-aminobutyric acid-A (GABA(A)) antagonist bicuculline. Ipsilateral disynaptic excitatory postsynaptic potentials (EPSPs) were analyzed as well. The functional organization of convergent monosynaptic and disynaptic excitatory and inhibitory inputs onto secondary VNs was studied by separate electrical stimulation of individual semicircular canal nerves on the ipsilateral side. Most secondary VNs (88%) received a monosynaptic EPSP exclusively from one of the three semicircular canal nerves; fewer secondary VNs (10%) were monosynaptically excited from two semicircular canal nerves; and even fewer secondary VNs (2%) were monosynaptically excited from each of the three semicircular canal nerves. Disynaptic EPSPs were present in the majority of secondary VNs (68%) and originated from the same (homonymous) semicircular canal nerve that activated a monosynaptic EPSP in a given neuron (22%), from one or both of the other two (heteronymous) canal nerves (18%), or from all three canal nerves (28%). Homonymous activation of disynaptic EPSPs prevailed (74%) among those secondary VNs that exhibited disynaptic EPSPs. Disynaptic inhibitory postsynaptic potentials (IPSPs) were mediated in 90% of the tested secondary VNs by glycine, in 76% by GABA, and in 62% by GABA as well as by glycine. These IPSPs were activated almost exclusively from the same semicircular canal nerve that evoked the monosynaptic EPSP in a given secondary VN. Our results demonstrate a canal-specific, modular organization of vestibular nerve afferent fiber inputs onto secondary VNs that consists of a monosynaptic excitation from one semicircular canal nerve followed by disynaptic excitatory and inhibitory inputs originating from the homonymous canal nerve. Excitatory and inhibitory second-order (secondary) vestibular interneurons are envisaged to form side loops that mediate spatially similar but dynamically different signals to secondary vestibular projection neurons. These feedforward side loops are suited to adjust the dynamic response properties of secondary vestibular projection neurons by facilitating or disfacilitating phasic and tonic input components.