An important part of the vestibule-ocular reflex is a group of cells i
n the caudal pens, known as the neural integrator, that converts eye-v
elocity commands, from the semicircular canals for example, to eye-pos
ition commands for the motoneurons of the extraocular muscles. Previou
sly, a recurrently connected neural network model was developed by us
that learns to simulate the signal processing done by the neural integ
rator, but it uses an unphysiological learning algorithm. We describe
here a new network model that can learn the same task by using a local
, Hebbian-like learning algorithm that is physiologically plausible. T
hrough the minimization of a retinal slip error signal the model learn
s, given randomly selected initial synaptic weights, to both integrate
simulated push-pull semicircular canal afferent signals and compensat
e for orbital mechanics as well. Approximately half of the model's 14
neurons are inhibitory, half excitatory. After learning, inhibitory ce
lls tend to project contralaterally, thus forming an inhibitory commis
sure. The network can, of course, recover from lesions. The mature net
work is also able to change its gain by simulating abnormal visual-ves
tibular interactions. When trained with a sine wave at a single freque
ncy, the network changed its gain at and near the training frequency b
ut not at significantly higher or lower frequencies, in agreement with
previous experimental observations. Commissural connections are essen
tial to the functioning of this model, as was the case with our previo
us model. In order to determine whether a commissure plays a similar r
ole in the real neural integrator, a series of electrical perturbation
s were performed on the midlines of awake, behaving juvenile rhesus mo
nkeys and the effects on the monkeys' eye movements were examined. Eye
movements were recorded using the coil system before, during, and aft
er electrical stimulation in the midline of the pens just caudal to th
e abducens nuclei, which reversibly made the integrator leaky. Eye mov
ements were also recorded from two of the monkeys before and after a m
idline electrolytic lesion was made at the location where stimulation
produced a leaky integrator. This lesion disabled the integrator irrev
ersibly. The eye movements that were produced by the monkeys as a resu
lt of these perturbations were then compared with eye movements produc
ed by the model after analogous perturbations. The results are compati
ble with the hypothesis that integration comes about by positive feedb
ack through lateral inhibition effected by an inhibitory commissure.