CANAL-SPECIFIC EXCITATION AND INHIBITION OF FROG 2ND-ORDER VESTIBULARNEURONS

Second-order vestibular neurons (2 degrees VNs) were identified in the in vitro frog brain by their monosynaptic excitation following electr ical stimulation of the ipsilateral VIIIth nerve. Ipsilateral disynapt ic inhibitory postsynaptic potentials were revealed by bath applicatio n of the glycine antagonist strychnine or of the gamma-aminobutyric ac id-A (GABA(A)) antagonist bicuculline. Ipsilateral disynaptic excitato ry postsynaptic potentials (EPSPs) were analyzed as well. The function al organization of convergent monosynaptic and disynaptic excitatory a nd inhibitory inputs onto 2 degrees VNs was studied by separate electr ical stimulation of individual semicircular canal nerves on the ipsila teral side. Most 2 degrees VNs (88%) received a monosynaptic EPSP excl usively from one of the three semicircular canal nerves; fewer 2 degre es VNs (10%) were monosynaptically excited from two semicircular canal nerves; and even fewer 2 degrees VNs (2%) were monosynaptically excit ed from each of the three semicircular canal nerves. Disynaptic EPSPs were present in the majority of 2 degrees VNs (68%) and originated fro m the same (homonymous) semicircular canal nerve that activated a mono synaptic EPSP in a given neuron (22%), from one or both of the other t wo (heteronymous) canal nerves (18%), or from all three canal nerves ( 28%). Homonymous activation of disynaptic EPSPs prevailed (74%) among those 2 degrees VNs that exhibited disynaptic EPSPs. Disynaptic inhibi tory postsynaptic potentials (IPSPs) were mediated in 90% of the teste d 2 degrees 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 2 degrees VN. Our results demonstrate a canal-specific, modular organization of vestibular nerve afferent fiber inputs onto 2 degrees VNs that consists of a monosynaptic excitation from one semicircular c anal nerve followed by disynaptic excitatory and inhibitory inputs ori ginating from the homonymous canal nerve. Excitatory and inhibitory se cond-order (2 degrees) vestibular interneurons are envisaged to form s ide loops that mediate spatially similar but dynamically different sig nals to 2 degrees vestibular projection neurons. These feedforward sid e loops are suited to adjust the dynamic response properties of 2 degr ees vestibular projection neurons by facilitating or disfacilitating p hasic and tonic input components.