The vestibular nuclei comprise a large set of neural elements in the brainstem that receive motion and other multisensory signals, then regulate movement responses and sensory experience. Many vestibular nuclei neurons have reciprocal connections with the cerebellum that form important regulatory mechanisms for the control of eye movements, head movements, and posture. There are four major vestibular nuclei that lie in the rostral medulla and caudal pons of the brainstem; all receive direct input from vestibular afferents (Brodal, 1984; Precht & Shimazu, 1965). Many of these nuclei neurons receive convergent motion information from the opposite ear through an inhibitory commissural pathway that uses gamma-aminobutyric acid (GABA) as a neurotransmitter (Kasahara & Uchino, 1974; Shimazu & Precht, 1966). The commissural pathway is highly organized such that cells receiving horizontal excitatory canal signals from the ipsilateral ear will also receive contralateral inhibitory horizontal canal signals from the opposite ear This fact gives rise to a “push-pull” vestibular function, whereby directional sensitivity to head movement is coded by opposing receptor signals. Because vestibular nuclei neurons receive information from bilateral inner ear receptors and because they maintain a high spontaneous firing rate (nearly 100 impulses/sec), they are thought to act to “compare” the relative discharge rates of left vs. right canal afferent firing activity. For example, during a leftward head turn, left brainstem nuclei neurons receive high firing-rate information from the left horizontal canal and low firing-rate information from the right horizontal canal. The comparison of activity is interpreted as a left head turn. Similar nuclei neuron responses exist when the head is pitched or rolled, with the vertical semicircular canals being stimulated by the rotational motion in their sensitivity planes. However, the opposing push-pull response from the vertical canals occurs with the anterior semicircular canal in one ear and the co-planar posterior semicircular canal of the opposite ear. Damage or disease that interrupts inner ear signal information from one side of the head can change the normal resting activity in the VIIIth nerve afferent fibers and will be interpreted by the brain as a head rotation, even though the head is stationary. These effects often lead to illusions of spinning or rotating that can be quite upsetting and may produce nausea or vomiting. However, over time the commissural fibers provide for vestibular compensation, a process by which the loss of unilateral vestibular receptor function is partially restored centrally and behavioral responses, such as the vestibuloocular reflex (VOR) and postural responses, mostly recover (Beraneck et al., 2003; Fetter & Zee, 1988,; Newlands, Hesse, Haque, & Angelaki, 2001; Newlands & Perachio, 1990).
In addition to the commissural pathway, many vestibular nuclei neurons receive proprioceptive signals from the spinal cord regarding muscle movement and position, visual signals regarding spatial motion, other multisensory (e.g., trigeminal) signals, and higher order signals from the cortex. It is thought that the cortical inputs regulate fine gaze and postural control, as well as suppress the normal compensatory reflexes during motion in order to elicit volitional movements. Of special significance are convergent signals from the semicircular canal and otolith afferents that allow central vestibular neurons to compute specific properties of head motion (Dickman & Angelaki, 2002). For example, Einstein (1907) showed that linear accelerations are equivalent whether they arise from translational motion or from tilts of the head relative to gravity. The otolith receptors cannot discriminate between the two, so how is it that we can tell the difference between when we are translating forward and tilting backward, where the linear acceleration signaled by the otolith afferents is the same? Vestibular nuclei and cerebellar neurons use convergent signals from both the semicircular canals and the otolith receptors to discriminate between tilt and translation, and as a result, some cells encode head tilt (Zhou, 2006) while other cells encode translational motion (Angelaki, Shaikh, Green, & Dickman, 2004).
Vestibuloocular system
The vestibular system is responsible for controlling gaze stability during motion (Crane & Demer, 1997). For example, if we want to read the sign in a store window while walking by, we must maintain foveal fixation on the words while compensating for the combined rotational and translational head movements incurred during our stride. The vestibular system regulates compensatory eye, neck, spinal, and limb movements in order to maintain gaze (Keshner & Peterson, 1995). One of the major components contributing to gaze stability is the VOR, which produces reflexive eye movements that are equal in magnitude and opposite in direction to the perceived head motion in 3D space (Wilson et al., 1995). The VOR is so accurate and fast that it allows people to maintain visual fixation on objects of interest while experiencing demanding motion conditions, such as running, skiing, playing tennis, and driving. In fact, gaze stabilization in humans has been shown to be completely compensatory (essentially perfect) for most natural behaviors. To produce the VOR, vestibular neurons must control each of the six pairs of eye muscles in unison through a specific set of connections to the oculomotor nuclei (Ezure & Graf, 1984). The anterior and posterior semicircular canals along with the saccule control vertical and torsional (turning of the eye around the line of sight) eye movements, while the horizontal canals and the utricle control horizontal eye movements.
To understand how the VOR works, let’s take the example of the compensatory response for a leftward head turn while reading the words on a computer screen. The basic pathway consists of horizontal semicircular canal afferents that project to specific neurons in the vestibular nuclei. These nuclei cells, in turn, send an excitatory signal to the contralateral abducens nucleus, which projects through the sixth cranial nerve to innervate the lateral rectus muscle (Figure 5). Some abducens neurons send an excitatory projection back across the midline to a subdivision of cells in the ipsilateral oculomotor nucleus, which, in turn, projects through the third cranial nerve to innervate the right (ipsilateral) medial rectus muscle. When a leftward head turn is made, the left horizontal canal vestibular afferents will increase their firing rate and consequently increase the activity of vestibular nuclei neurons projecting to the opposite (contralateral) right abducens nucleus. The abducens neurons produce contraction of the right lateral rectus and, through a separate cell projection to the left oculomotor nucleus, excite the left medial rectus muscles. In addition, matching bilateral inhibitory connections relax the left lateral rectus and right medial rectus eye muscles. The resulting rightward eye movement for both eyes stabilizes the object of interest upon the retina for greatest visual acuity.
Figure 5. Vestibuloocular reflex. During a leftward head turn, the left horizontal semicircular canal receptors are excited, while the right ear receptors are inhibited. The left excitatory signals excite vestibular nuclei neurons. These cells project across the brain to excite motor neurons in the right abducens nucleus (VI) that excite the lateral rectus muscle of the right eye and to cells in the oculomotor nucleus (III) that excite the medial rectus muscle of the left eye. This moves both eyes to the right to exactly match the leftward head movement and stabilize visual gaze upon a target of interest. The right ear inhibitory signals cross to neurons in the left vestibular nucleus that decrease their firing rate. These cells are inhibitory and decrease their firing rate to further increase the response of rightward motor eye muscle cells.
During linear translations, a different type of VOR also occurs (Paige & Tomko, 1991). For example, sideways motion to the left results in a horizontal rightward eye movement to maintain visual stability on an object of interest. In a similar manner, vertical up–down head movements (such as occur while walking or running) elicit oppositely directed vertical eye movements (Angelaki, McHenry, & Hess, 2000). For these reflexes, the amplitude of the translational VOR depends on viewing distance. This is due to the fact that the vergence angle (i.e., the angle between the lines of sight for each eye) varies as a function of the inverse of the distance to the viewed visual object (Schwarz, Busettini, & Miles, 1989). Visual objects that are far away (2 meters or more) require no vergence angle, but as the visual objects get closer (e.g., when holding your finger close to your nose), a large vergence angle is needed. During translational motion, the eyes will change their vergence angle as the visual object moves from close to farther away (or vice versa). These responses are a result of activation of the otolith receptors, with connections to the oculomotor nuclei similar to those described above for the rotational vestibuloocular reflex. With tilts of the head, the resulting eye movement is termed torsion, and consists of a rotational eye movement around the line of sight that is in the direction opposite to the head tilt. As mentioned above, there are major reciprocal connections between the vestibular nuclei and the cerebellum. It has been well established that these connections are crucial for adaptive motor learning in the vestibuloocular reflex (Lisberger, Pavelko, & Broussard, 1994).
The Vestibular System by Dora Angelaki and J. David Dickman is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. Permissions beyond the scope of this license may be available in our Licensing Agreement.
