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.