Three classes of vestibular-related neurons were found in and near the prep
ositus and medial vestibular nuclei of alert or decerebrate gerbils, those
responding to: horizontal translational motion, horizontal head rotation, o
r both. Their distribution ratios were 1:2:2, respectively. Many cells resp
onsive to translational motion exhibited spatiotemporal characteristics wit
h both response gain and phase varying as a function of the stimulus vector
angle. Rotationally sensitive neurons were distributed as Type I, II, or I
II responses (sensitive to ipsilateral, contralateral, or both directions,
respectively) in the ratios of 4:6:1. Four tested factors shaped the respon
se dynamics of the sampled neurons: canal-otolith convergence, oculomotor-r
elated activity, rotational Type (I or II), and the phase of the maximum re
sponse. Type I nonconvergent cells displayed increasing gains with increasi
ng rotational stimulus frequency (0.1-2.0 Hz, 60 degrees/s), whereas Type I
I neurons with convergent inputs had response gains that markedly decreased
with increasing translational stimulus frequency (0.25-2.0 Hz, +/- 0.1 g).
Type I convergent and Type II nonconvergent neurons exhibited essentially
flat gains across the stimulus frequency range. Oculomotor-related activity
was noted in 30% of the cells across all functional types, appearing as bu
rst/pause discharge patterns related to the fast phase of nystagmus during
head rotation. Oculomotor-related activity was correlated with enhanced dyn
amic range compared with the same category that had no oculomotor-related r
esponse. Finally, responses that were in-phase with head velocity during ro
tation exhibited greater gains with stimulus frequency increments than neur
ons with out-of-phase responses. In contrast, for translational motion, neu
rons out of phase with head acceleration exhibited low-pass characteristics
, whereas in-phase neurons did not. Data from decerebrate preparations reve
aled that although similar response types could be detected, the sampled ce
lls generally had lower background discharge rates, on average one-third lo
wer response gains, and convergent properties that differed from those foun
d in the alert animals. On the basis of the dynamic response of identified
cell types, we propose a pair of models in which inhibitory input from vest
ibular-related neurons converges on oculomotor neurons with excitatory inpu
ts from the vestibular nuclei. Simple signal convergence and combinations o
f different types of vestibular labyrinth information can enrich the dynami
c characteristics of the rotational and translational vestibuloocular respo
nses.