The left vestibular afferent fibers are stimulated by the depolarized hair cells, resulting in increased activity. This excites the neurons in the left medial vestibular nucleus, which include excitatory neurons that project to the contralateral abducens nucleus. These neurons synapse with both motor neurons and internuclear neurons. The excitation of motor neurons leads to the contraction of the right lateral rectus muscle, causing the right eye to rotate to the right. The excitation of internuclear neurons in the right abducens nucleus leads to the excitation of the medial rectus motor neurons in the left oculomotor nucleus, causing the left eye to rotate to the right as well.

Along the pathway starting with the inhibitory vestibular neurons, which project from the left medial vestibular nucleus to the ipsilateral abducens nucleus, the activity of these cells inhibits the motor neurons to the left lateral rectus muscle and the motor neurons to the right medial rectus muscle. This relaxation of the muscles facilitates rotation of the eyes to the right. Therefore, the eye is pulled by the increased tension in one set of muscles and "pushed" by the release of tension in the antagonist set of muscles.

It should be noted that the mirror image pathways originating from the right canal are not shown for clarity. However, the changes in activity through these pathways with leftward head rotation would be exactly the opposite and would function synergistically with those shown. The resulting changes in activity through these circuits can be worked out as an exercise. Leftward head rotation hyperpolarizes the hair cells of the right canal, leading to a decrease in right vestibular afferent activity and disfacilitation of the right vestibular nuclear neurons.

Now, let's consider the commissural fibers that connect the two medial vestibular nuclei. These fibers are excitatory and end on local inhibitory interneurons of the contralateral vestibular nucleus, inhibiting the projection neurons of that nucleus. This pathway reinforces the actions of the contralateral vestibular afferent fibers on their target vestibular nuclear neurons. In the given example, the commissural cells in the left vestibular nucleus are activated, causing active inhibition of the right medial vestibular nuclei projection neurons. This reinforcement adds to the disfacilitation caused by the decrease in right afferent activity. It is important to note that this commissural pathway is powerful enough to modulate the activity of the contralateral vestibular nuclei even after unilateral labyrinthectomy, which destroys the direct vestibular afferent input to these nuclei.

In addition to the brainstem circuits, the cerebellum plays a role in the vestibulo-ocular reflex (VOR). Parts of the vermis and flocculonodular lobe receive primary vestibular afferent fibers or secondary vestibular afferent fibers, or both. These fibers project back to the vestibular nuclei directly and via a disynaptic pathway involving the fastigial nucleus. The exact role of these cerebellar circuits in generating the VOR is subject to debate, but they are critical as damage to them leads to abnormal eye movement, such as spontaneous nystagmus, and other symptoms of vestibular dysfunction.
Fig. 8.27 ). The depolarized hair cells cause increased activity in the left vestibular afferent fibers and thereby excite neurons of the left medial vestibular nucleus. These include excitatory neurons that project to the contralateral abducens nucleus and synapse with both motor neurons and internuclear neurons. Excitation of the motor neurons leads to contraction of the right lateral rectus muscle and rotation of the right eye to the right, whereas excitation of the internuclear neurons of the right abducens nucleus leads to excitation of the medial rectus motor neurons in the left oculomotor nucleus, thus causing the left eye to rotate to the right as well.
Along the pathway starting with the inhibitory vestibular neurons that project from the left medial vestibular nucleus to the ipsilateral abducens nucleus, the activity of these cells leads to inhibition of motor neurons to the left lateral rectus muscle and motor neurons to the right medial rectus muscle (the latter via internuclear neurons to the right oculomotor nucleus). Consequently, these muscles relax, thereby facilitating rotation of the eyes to the right. Thus the eye is being pulled by the increased tension of one set of muscles and “pushed” by the release of tension in the antagonist set of muscles.
Note again that the mirror image pathways originating from the right canal have been left out of
Fig. 9.27 for clarity, but the changes in activity through them with leftward head rotation would be exactly the opposite, and thus they would function synergistically with those that are shown. As an exercise, work out the resulting changes in activity through these circuits. Remember that leftward head rotation hyper-polarizes the hair cells of the right canal, thereby leading to a decrease in right vestibular afferent activity and disfacilitation of the right vestibular nuclear neurons.
Now, consider the commissural fibers that connect the two medial vestibular nuclei are excitatory but end on local inhibitory interneurons of the contralateral vestibular nucleus and thus inhibit the projection neurons of that nucleus. This pathway reinforces the actions of the contra-lateral vestibular afferent fibers on their target vestibular nuclear neurons. In the aforementioned example, commissural cells in the left vestibular nucleus are activated and therefore cause active inhibition of the right medial vestibular nuclei projection neurons, which reinforces the disfacilitation caused by the decrease in right afferent activity. In fact, this commissural pathway is powerful enough to modulate the activity of the contralateral vestibular nuclei even after unilateral labyrinthectomy, which destroys the direct vestibular afferent input to these nuclei.
Of importance is that superimposed on the brainstem circuits is the cerebellum. Parts of the vermis and flocculonodular lobe receive primary vestibular afferent fibers or secondary vestibular afferent fibers (axons of the vestibular nuclear neurons), or both, and in turn project back to the vestibular nuclei directly and via a disynaptic pathway involving the fastigial nucleus. The exact role of these cerebellar circuits in generating the VOR is much debated, but they are critical inasmuch as damage to them leads to abnormal eye movement, such as spontaneous nystagmus, and other symptoms of vestibular dysfunction.