Horizontal semicircular canal function

The vestibular system is composed of 2 types of sensory organs (the semicircular canals and the otolith organs) that contribute to gaze and postural stability. Three semicircular canals (superior, posterior, and horizontal) are positioned orthogonally to each other to sense rotational head movement or angular acceleration in the yaw, pitch, and roll planes. For example, the purpose of the horizontal semicircular canals is to provide sensory input to the vestibuloocular reflex (VOR) regarding head rotation in the yaw (horizontal) plane. The primary goal of the semicircular canals is to provide input via the VOR for gaze stability when the head is in motion. The horizontal VOR, therefore, contributes to gaze stability when the head is rotated laterally. Clinical tests of horizontal semicircular canal function have been widely available for many years and include the bithermal binaural caloric test and rotational tests. These tests have been the predominant measure of vestibular function in studies examining the effects of head injury on the vestibular system.

It is well established that head injury can result in peripheral vestibular hypofunction (or unilateral weakness on the caloric test), and it is reasonable to presume that peripheral vestibular system abnormalities associated with TBI are likely due to the head injury rather than the resulting brain injury. Reports reveal that the incidence of horizontal semicircular canal (VOR) dysfunction ranges from 32% to 71% in patients with dizziness after head injury. Davies and Luxon performed electronystagmography testing on 100 consecutive patients who experienced dizziness after head injury and reported that 71% had positive vestibular test findings that included abnormal calorics, the presence of spontaneous nystagmus, or both. Similarly, Toglia and colleagues reported a high incidence of abnormal calorics (63%) and spontaneous nystagmus in patients with head injury. In contrast, Gannon and colleagues reported abnormal vestibular findings in 32% of patients with head injury.

A few studies have examined the effect of blast exposure on horizontal semicircular canal function, and the findings have been inconclusive. Shupak and colleagues examined 5 patrol boat crew members who were injured by close-range explosion of a trinitrotoluene device. The investigators reported that 2 crew members had vestibular abnormalities on tests of horizontal canal function (caloric weakness and/or phase lead on rotary chair) and 1 crew member had BPPV and spontaneous nystagmus. In contrast, Cohen and colleagues reported no caloric abnormalities in 7 survivors who complained of dizziness after a suicide terrorist attack on a municipal bus in Israel. Van Campen and colleagues measured vestibular function using the caloric test in 30 survivors of the Oklahoma City Federal Building bombing who had complaints of dizziness or imbalance. Only 2 survivors demonstrated abnormal caloric findings, and 8 had positional/spontaneous nystagmus.

Otolith organ function

Two otolith organs sense linear acceleration, head tilt, and gravity, with the primary function to provide input for postural stability via the vestibulospinal tract. The otolith organs are composed of the saccule and the utricle that contribute to postural stability by providing sensory input regarding linear acceleration and changes in gravity. In an upright position, the saccule is positioned vertically and senses linear acceleration in the vertical plane. In contrast, the utricle is positioned horizontally (3.5–4 cm from midline) and senses linear acceleration in the lateral plane. Both the utricle and the saccule respond to acceleration in the anterior-posterior plane.

Until recently, tests to measure otolith function have been used experimentally rather than clinically. Experimental methods include the measurement of the otolith-ocular response during stimulation of the otolith organs with linear acceleration using parallel sleds and swings. However, these methods of otolith stimulation are cumbersome and not sensitive to unilateral otolith hypofunction; therefore, their use has been limited to experimental purposes. More recently, research has focused on the development of clinical tests of otolith function. The cervical vestibular evoked myogenic potential (cVEMP) has been established as a clinical test of saccular and/or inferior vestibular nerve function. cVEMPs are short latency electrical potentials evoked by high-level acoustic stimuli recorded from surface electrodes over the tonically contracted sternocleidomastoid (SCM) muscle. The cVEMP waveform consists of an early positive-negative component that depends on the integrity of vestibular afferents because it is abolished after vestibular nerve section but preserved in subjects with severe to profound sensorineural hearing loss. The neurophysiological and clinical data indicate that cVEMPs are mediated by an ipsilateral pathway that includes the saccular macula, inferior vestibular nerve, vestibular nucleus, medial vestibulospinal tract, and motoneurons of the SCM muscle.

The subjective visual vertical (SVV) test has been used as a clinical test of utricular function. The SVV angle is the angle between the gravitational axis (true earth vertical) and the position of a visual linear marker adjusted vertically by a subject. The otolith organs contribute to the estimation of the physical vertical orientation, and normal subjects align the SVV angle within 2° of true vertical (0°). Impaired SVV test results have been documented in patients with unilateral vestibular disorders and in patients with central vestibular disorders, such as brainstem and thalamic infarctions. The SVV angle can also be measured during off-axis yaw rotation to the right or left (unilateral centrifugation) to measure ear-specific utricular function and determine chronic (compensated) vestibular dysfunction. In individuals with normal vestibular function, the SVV angle tilts symmetrically during unilateral centrifugation. That is, when the subject is positioned to the right side of the axis of rotation, the SVV is tilted toward the left, and when the subject is positioned to the left side of the axis of rotation, the SVV is tilted in a similar magnitude to the right. Patients with chronic unilateral vestibular loss exhibit an SVV asymmetry when measured during off-axis (eccentric) yaw rotation. Specifically, when the lesioned ear is centrifuged, the SVV angle does not shift because the utricle does not respond to the gravitoinertial force vector (linear acceleration).

Both circumstantial and direct evidence suggest that otolith function may be compromised by head trauma.

First, Schuknecht and Davison reported damage to the membranous walls of the utricle and saccule and degenerative changes in the saccular macula in a cat after multiple blows to an unrestrained head. The investigators theorized that the linear acceleration and deceleration of the head blow damaged the otolith organs that sense linear acceleration. Similarly, a histologic study of 10 human victims of a bomb blast demonstrated rupture of the saccule and utricle.

Second, numerous studies have determined that BPPV occurs in 10% to 25% of head trauma patients, and it is presumed that a blow to the head dislodges otoconia from the utricular otolithic membrane, resulting in free-floating particles (otoconia) that produce endolymphatic fluid flow in the semicircular canals (canalithiasis). Davies and Luxon performed audiovestibular testing on 100 consecutive patients with a history of head injury and determined that audiovestibular organs are interdependently vulnerable to trauma, but the otolith organs are the most vulnerable because of the high incidence of BPPV.

Third, some patients with head injury experience dizziness and imbalance yet have normal horizontal semicircular canal test findings.

Finally, postural instability or imbalance is a common symptom in patients with head trauma, and the otolith organs contribute to postural stability by serving as gravity sensors to the vestibulospinal pathways.

Ernst and colleagues provided the most direct and compelling evidence that otolithic involvement is a common sequela of head trauma by demonstrating a high incidence of cVEMP and SVV abnormalities, in patients with head injury. Furthermore, Basta and colleagues determined that postural stability was correlated with otolith disturbances in patients with mild blunt head injury. Because the vestibulospinal reflex (VSR) uses otolith input to a greater extent than the VOR, this finding is not surprising and suggests that otolith disorders are a likely source of posttraumatic imbalance.

Otolith organ function

Two otolith organs sense linear acceleration, head tilt, and gravity, with the primary function to provide input for postural stability via the vestibulospinal tract. The otolith organs are composed of the saccule and the utricle that contribute to postural stability by providing sensory input regarding linear acceleration and changes in gravity. In an upright position, the saccule is positioned vertically and senses linear acceleration in the vertical plane. In contrast, the utricle is positioned horizontally (3.5–4 cm from midline) and senses linear acceleration in the lateral plane. Both the utricle and the saccule respond to acceleration in the anterior-posterior plane.

Until recently, tests to measure otolith function have been used experimentally rather than clinically. Experimental methods include the measurement of the otolith-ocular response during stimulation of the otolith organs with linear acceleration using parallel sleds and swings. However, these methods of otolith stimulation are cumbersome and not sensitive to unilateral otolith hypofunction; therefore, their use has been limited to experimental purposes. More recently, research has focused on the development of clinical tests of otolith function. The cervical vestibular evoked myogenic potential (cVEMP) has been established as a clinical test of saccular and/or inferior vestibular nerve function. cVEMPs are short latency electrical potentials evoked by high-level acoustic stimuli recorded from surface electrodes over the tonically contracted sternocleidomastoid (SCM) muscle. The cVEMP waveform consists of an early positive-negative component that depends on the integrity of vestibular afferents because it is abolished after vestibular nerve section but preserved in subjects with severe to profound sensorineural hearing loss. The neurophysiological and clinical data indicate that cVEMPs are mediated by an ipsilateral pathway that includes the saccular macula, inferior vestibular nerve, vestibular nucleus, medial vestibulospinal tract, and motoneurons of the SCM muscle.

The subjective visual vertical (SVV) test has been used as a clinical test of utricular function. The SVV angle is the angle between the gravitational axis (true earth vertical) and the position of a visual linear marker adjusted vertically by a subject. The otolith organs contribute to the estimation of the physical vertical orientation, and normal subjects align the SVV angle within 2° of true vertical (0°). Impaired SVV test results have been documented in patients with unilateral vestibular disorders and in patients with central vestibular disorders, such as brainstem and thalamic infarctions. The SVV angle can also be measured during off-axis yaw rotation to the right or left (unilateral centrifugation) to measure ear-specific utricular function and determine chronic (compensated) vestibular dysfunction. In individuals with normal vestibular function, the SVV angle tilts symmetrically during unilateral centrifugation. That is, when the subject is positioned to the right side of the axis of rotation, the SVV is tilted toward the left, and when the subject is positioned to the left side of the axis of rotation, the SVV is tilted in a similar magnitude to the right. Patients with chronic unilateral vestibular loss exhibit an SVV asymmetry when measured during off-axis (eccentric) yaw rotation. Specifically, when the lesioned ear is centrifuged, the SVV angle does not shift because the utricle does not respond to the gravitoinertial force vector (linear acceleration).

Both circumstantial and direct evidence suggest that otolith function may be compromised by head trauma.

First, Schuknecht and Davison reported damage to the membranous walls of the utricle and saccule and degenerative changes in the saccular macula in a cat after multiple blows to an unrestrained head. The investigators theorized that the linear acceleration and deceleration of the head blow damaged the otolith organs that sense linear acceleration. Similarly, a histologic study of 10 human victims of a bomb blast demonstrated rupture of the saccule and utricle.

Second, numerous studies have determined that BPPV occurs in 10% to 25% of head trauma patients, and it is presumed that a blow to the head dislodges otoconia from the utricular otolithic membrane, resulting in free-floating particles (otoconia) that produce endolymphatic fluid flow in the semicircular canals (canalithiasis). Davies and Luxon performed audiovestibular testing on 100 consecutive patients with a history of head injury and determined that audiovestibular organs are interdependently vulnerable to trauma, but the otolith organs are the most vulnerable because of the high incidence of BPPV.

Third, some patients with head injury experience dizziness and imbalance yet have normal horizontal semicircular canal test findings.

Finally, postural instability or imbalance is a common symptom in patients with head trauma, and the otolith organs contribute to postural stability by serving as gravity sensors to the vestibulospinal pathways.

Ernst and colleagues provided the most direct and compelling evidence that otolithic involvement is a common sequela of head trauma by demonstrating a high incidence of cVEMP and SVV abnormalities, in patients with head injury. Furthermore, Basta and colleagues determined that postural stability was correlated with otolith disturbances in patients with mild blunt head injury. Because the vestibulospinal reflex (VSR) uses otolith input to a greater extent than the VOR, this finding is not surprising and suggests that otolith disorders are a likely source of posttraumatic imbalance.

Central vestibular system/CNS function

Sensory input to the vestibular sensory organs and nerves is processed by the central vestibular system, and the origin for dizziness can occur anywhere along these pathways. The central vestibular system includes the brainstem and cerebellum, but pathways also project to higher centers in the midbrain and cerebral cortex. Ocular motor testing can be used as a screening measure for determining CNS function independent from peripheral vestibular system function. In addition, fixation suppression of vestibular nystagmus requires intact connections between the cerebellum and vestibular nuclei and thus has been used as a clinical test for central vestibular involvement. Many CNS disorders cause gaze-evoked nystagmus that can be observed during clinical assessment.

It has been proposed that unsteadiness or imbalance related to head injury is due to central involvement when tests of horizontal semicircular canal (eg, caloric test) or auditory function are within normal limits. There is evidence, however, that suggests central vestibular involvement is less common than peripheral involvement in patients after head injury. Davies and Luxon found that only 8 of 100 patients had central findings that included either abnormal ocular motor tests and/or incomplete vestibular suppression. In contrast, Tuohimaa reported a high incidence of central disturbances in patients shortly after head trauma (60%), although the patients with central findings were older than the patients without central findings and the incidence of central involvement decreased to 12% at 6 months after the head trauma.

To the authors’ knowledge, central vestibular pathology has not been investigated in victims of blast exposure. Animal studies have determined enlarged ventricles, minor bleeding, and diffuse axonal injury resulting from primary blast injury, although few clinical studies have examined the effects of blast on the human brain. Recent developments in neuroimaging techniques may lead to the development of biomarkers for blast-related TBI.