Introduction to Concussions and Vestibular Rehabilitation

Concussion is defined by the collection of symptoms associated with impact to the head, face, neck or elsewhere in the body such that a mechanical force is transmitted to the brain. Also referred to as mild traumatic brain injury (MTBI), concussive injuries cause symptoms of vestibular impairment in 30-65% of patients. Individuals who obtain concussions often suffer from postconcussion syndrome following the initial injury. Signs and symptoms that may present in this syndrome include headaches, dizziness, vertigo, light and noise sensitivity, diplopia, impaired senses, changes in mood or mental state, changes in sleep patterns, and impaired cognition and memory.

Dizziness, impaired balance, and blurred vision are among the most commonly observed symptoms postconcussion. Possible causes of these symptoms include benign paroxysmal positional vertigo (BPPV), labyrinthine concussion, perilymphatic fistula, post-traumatic Mienere syndrome, temporal bone fracture, cervical vertigo, epileptic vertigo, migraine associated vertigo, and ocular-motor abnormalities. If physiological symptoms persist for more than seven days after injury, seeking further treatment is advised, commonly in the form of vestibular rehabilitation therapy (VRT) with a physical therapist. The goal of VRT is to design a program consisting of exercises and movements aimed at improving balance deficiencies, decreasing dizziness, increasing activity level, and improving the individual's general ability to function. Exercises used in VRT include the canalith repositioning maneuver, habituation, adaptation, substitution, balance exercises, and aerobic exercises. VRT has been shown to successfully improve symptoms of dizziness, gaze instability, and balance dysfunction in post-concussive vestibular patients.


Anatomical Review of the Vestibular System

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Figure 1: The structures within the membranous labyrinth.
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Figure 2: Sensors of the otolithic organs and semicircular canals.


The vestibular system is comprised of three functional units: two labyrinths (the peripheral sensory apparatus), the vestibular nuclear complex and cerebellum (the primary and central processors), and motor neurons (the mechanism for motor output). One labyrinth is located in each inner ear, and is made up of three semicircular canals (SCC), the vestibule (containing the two otolithic organs), and the cochlea.

The semicircular canals provide information regarding angular head motion and velocity. Each labyrinth contains three canals--the anterior, posterior and lateral--and the each canal works in a coplanar pair with a canal of the other labyrinth (right and left lateral canals, left anterior and right posterior canals, and left posterior and right anterior canals). At the anterior opening of the horizontal and anterior canals and the inferior opening of the posterior canal, a structure termed the ampulla forms. The ampulla sits atop the crista, a septum of supporting tissue, from which hair cells emerge to protrude their cilia into the membranous cupula. Upon angular motion of the head, endolymphatic fluid within the canal is displaced, causing the cupula to bend and stimulate the innervating hair cells.

The otolithic organs, comprising of the saccule and utricle, provide information regarding linear acceleration of the head. The saccule responds to motion in the vertical plane, while the utricle responses to motion in the horizontal plane. Within each otolithic organ, maculae, located on the medial wall of the saccule and the floor of the utricle, innervate the otoconia-containing otolithic membrane. Much like in the canals, movement of the endolymph within the organs displaces the membranous structure, stimulating the hair cells innervating it.


Anatomy of Vertigo Symptoms

Vertigo, an illusion of movement, is a commonly seen type of dizziness. Benign paroxysmal positional vertigo (BPPV), the most common cause of vertigo, is the result of an abnormal stimulation of one of the semicircular canals. Two theories present as explanation for BPPV: the cupulolithiasis theory, and the canalithiasis theory.
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Figure 3: The Dix-Hallpike Test for BPPV.
In the cupulolithiasis theory, otoconia in the utricle become detached and inferiorly descend into the labyrinth traveling into a semicircular canal (most commonly the posterior), where they become attached to the cupula. The replacement of the otoconia causes the canal entered to become sensitive to gravity when the head is in a position relevant to the canal, causing false stimulations about head position to be fired. The canalithiasis theory, however, states that degenerating otoconia or some other debris becomes free-floating in the canal endolymph, resulting in any any head movement change relevant to canal orientation causing a movement of the particles within the canal. This movement of particles disturbs the endolymph and stimulates the ampulla; the stimulation lasts as long as the particles continue to move. Moreover, symptoms due to BPPV occur directly following a critical change in position then settle after some time, but will be provoked again any time the position changes in a significant manner.
Although both explanations for post-trauma related vertigo are still recognized, the canalithiasis theory is currently more accepted by clinicians and professionals. Due to the structure and positioning of the otolithic organs in relation to the semicircular canals, the otoconial debris may not enter into the canal arm until the individuals head moves into the critical position; because of this, the onset of positional vertigo symptoms may be delayed following injury to the head. Alternatively, damage to the afferent vestibular nerve may also produce a false sensation of angular rotation, resulting in vertigo symptoms.


Vestibular Pathways

Labyrinthine Outputs

Scarpa's (vestibular) ganglion, found at the distal portion of the internal auditory meatus, gives rise to the cell bodies of the 1st order afferents of the peripheral vestibular sensory organs. The neurons of the vestibular ganglion are bipolar; one branch innervates the peripheral hair cell receptors of the semicircular canals and otoliths, while the other travels to structures of the brain. The vestibular nerve has two parts innervating the sensory receptors of the labyrinth: the superior vestibular nerve, carrying information from the utricle and horizontal and anterior canals, and the inferior vestibular nerve, carrying information from the saccule and posterior canal. After traveling from Scarpa's ganglion via the vestibulocochlear nerve (cranial nerve VIII), the axons of the vestibular nerve enter the brainstem at the pontomedullary junction. Once entered the brainstem, most of the afferents project to vestibular nuclei in the rostral medulla and caudal pons, while some travel directly to the cerebellum.

The vestibular nuclei complex consists of the lateral, medial, superior and inferior vestibular nuclei. As the primary processors for vestibular input, these nuclei are responsible for receiving and then sending out the afferent information from the vestibular receptors. From these nuclei, projections are made to the spinal cord, the extraocular motor nuclei, the cerebellum, and the thalamus. Through these connections, input from the vestibular system plays a role in the control of head and body position, the control of eye movements, postural adjustments, and movement perception.


Pathways Associated with Vestibular Impairment

Symptoms attributable to the vestibular system following head injury my collaboratively lead to a generalized disorientation. Vestibular impairment may specifically influence an individual's ability to maintain posture and balance, as well as affect the control of reflexive eye movements. Decreased balance in patients with concussions may be attributable to the vestibular systems afferent connections to the vestibulospinal tracts, originating at the medial and lateral vestibular nuclei. With contralateral synapses on interneurons of axial musculature, these tracts serve as the direct pathway for the vestibular influence on body posture. Therefore, altered signals from the vestibular afferents may incorrectly influence ones posture, changing balance ability. The vestibuloocular reflex (VOR) is a compensatory eye movement, responsible for maintaining a stable image during head movements by moving the eyes at the same speed as the head, but in the opposite direction. Vestibular innervation of this reflex lies in the control of the extraocular muscles through ipsilateral connections of the lateral vestibular nucleus and medial longitudinal fasciculus with the oculomotor nuclei. The loss of accuracy in control of the VOR may lead to blurred vision, false perception of movement, and dizziness.


Post-Concussive VRT

Evaluation of vestibular system pathology includes assessments of vertigo, head-eye coordination, and neural components of postural and stability control. Through administration of an exercise program, VRT seeks to decrease symptoms, improve vestibular connections, and retrain vestibular-related impairments that follow MTBI. Exercises are designed with the intent to facilitate compensation of vestibular dysfunction through means of the central nervous system adaptation.

The Cantu Concussion Grading Guidelines uses assessment of post-concussive signs and symptoms to grade concussion severity. Most commonly used in sport-induced concussions, the reference guidelines also provide protocol and instructions for return to activity for athletes following injury. Until recently, the Cantu Guidelines was one of the most widely known and referred-to grading scales for sport-related concussions; its use decreased in the past few years when the use of concussion-severity grading systems were abandoned by the American Academy of Neurology.

Assessment and Treatment: BPPV

In a patient who presents with dizziness, BPPV is in most cases the first vestibular disorder tested for. The Dix-Hallpike Test (figure 3) identifies BPPV in the posterior or anterior semicircular canals by having the patient turn their head, then quickly go from a sitting to a lying position; symptoms of vertigo immediately following the change in position is a positive indication of BPPV. To test the horizontal canals, clinicians administer the Roll Test; here, the patient lies on their back with their head slightly flexed. The clinician quickly rotates their head to one side, then after about a minute returns the head to it's original position, before producing the same rotation to the other side. A positive test provokes symptoms with head rotations in both directions.
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Figure 4: The canalith repositioning maneuver.

The canalith repositioning maneuver (CRM) developed by John Epley is the most popular method used by clinicians for relocation of displaced otoconia, particularly in the case of canalithiasis. In this method of treatment, the goal is to remove the otolithic debris from the canal by creating a rotating of endolymph toward the canal opening so that upon sitting up, the debris will re-enter the utricle, where they will either dissolve into the endolymph or be taken up into the gelatinous membrane. The maneuver is started with the patient in the Dix-Hallpike position in which symptoms are provoked. After a minute, the administrator momentarily rotates the patient's head toward the unaffected side, before having the patient roll onto that side with their head rotated downward. The patient is then instructed to slowly sit up while keeping their head in the previous rotated position. In most cases, patients are relieved of vertigo symptoms after a single treatment, making the CRM the most effective and successful treatment for BPPV. The patient is likely to experience brief vertigo following each positional change during the maneuver; in the patient with high levels of nausea, taking a vestibular-suppressant medication prior to the maneuver may be recommended to prevent extreme nausea or vomiting. Alternatively, and less commonly used, the liberatory maneuver is used for BPPV caused by cupulothiasis. Brandt-Daroff habituation exercises may be issued for mild, residual symptoms following either of the mentioned maneuvers.

Assessment and Treatment: Head-Eye Coordination

Assessment of movements specific to head-eye coordination looks at eye movements in respect to a moving visual target or shift of visual targets, and reflexive movements of the eye intended to maintain a stable visual image during head movements. Specific eye movements and reflexes commonly assessed include smooth pursuit, saccadic eye movements, and the VOR. Examiners look for increases in symptoms associated with with specific eye movement, including those of dizziness, blurred vision, and oscillopsia.

A progressive set exercises that increase in coordination complexity is to improve gaze stabilization and decrease associated symptoms. Therapists will initially perform saccadic and smooth pursuit track exercises, where the seated patient is instructed to follow a moving target in their visual field, or change their fixation between two or more targets. Once the patient has reached a point where these exercises provoke little-to-no symptoms, the therapist will move forward with instructing VOR-dependent exercises. These exercises begin to focus more on gaze stabilization, as the patient is told to maintain a fixed gaze on a target in the center of their visual field while moving their head back-and-forth. Once the patient has again reached a point where the exercises trigger minimal symptoms, the next step is to go through the progression of these exercises, first while standing, and then while walking when appropriate. All exercises should be performed in both the vertical and horizontal directions for best results.

Assessment and Treatment: Postural Control, Stability and Balance

To accurately evaluate a patient's stability, assessment must be multi-dimensional, examining multiple systems. The Berg Balance Scale, which rates fourteen different tasks on a scale of 0-4, has shown to have high reliability in assessment of balance in patients with MTBI. The Dynamic Gait Index, which tests eight tasks on a scale of 0-3, is used to evaluate a patient's ability to adapt their gait to changing task demands. In addition to these two rating-based assessments of functional mobility, evaluation of balance and mobility associated with dual-tasks is believed to be important in proper assessment.

To treat postural instability, exercises aimed to improve sensory function for orientation are prescribed. Most commonly, patients will be given balance exercises that will continually increase in difficulty. The therapist may have the patient perform certain movements, or limit their sensory input by having them close their eyes, while maintaining a specific foot-placement or balance on one leg. By decreasing visual input availability, therapists are able to instigate the improvement of vestibular inputs for postural control.


Conclusion

Over recent decades, the medical topic of concussions has gained increasingly more attention, and the knowledge regarding injury recognition, diagnosis and treatment that we have accessible continues to grow. As an injury to the most complex part of the human body, symptoms, impairments and treatments following concussion spread much further than what we have discussed here. In addition to the commonly experienced vestibular symptoms of dizziness, impaired balance and blurry vision, many other physiological symptoms may present following MTBI. Patients may also experience cognitive-psychological symptoms, including deficits in concentration, comprehension and memory function. Treatment under a neuropsychologist or other cognitive-concussion specialist may be necessary if symptoms impairing normal mental function persist.


Glossary

Concussion: a blow to the head, which may or may not be accompanied by some period of unconsciousness, that results in few to many symptoms lasting anywhere from several hours to weeks.
Vestibular rehabilitation therapy (VRT): a form of physical therapy aimed to address vestibular system dysfunction through exercises.
Labyrinth: made up of a bony and membranous part; located within the petrous portion of the temporal bone and contains the auditory and vestibular sensory organs.
Semicircular canal (SCC): 3 in each labyrinth (the superior, inferior, and horizontal); vestibular organs responsible for detecting angular (pitch/yaw/roll) movements of the head.
Ampulla: the widened opening for each of the semicircular canals, containing sensory innervations.
Cupula: a gelatinous membrane innervated by cilia in the canals.
Saccule: the otolithic organ responsible for detection of vertical accelerations of the head.
Utricle: the otolithic organ responsible for detection of horizontal accelerations of the head.
Otoconia: small calcium carbonate crystals embedded into the otolithic membrane.
Benign paroxysmal positional vertigo (BPPV): a type of vertigo caused either by movement of detached otoconia within the inner ear or otoconia adherent to the cupula.
Vestibulo-ocular reflex (VOR): generates eye movements that enable clear vision while the head is in motion.
Dix-Hallpike Test: the most commonly used test for confirmation of BPPV diagnosis.
Roll Test: tests for horizontal canal BPPV; often follows Dix-Hallpike no symptoms have been provoked.
Canalith repositioning maneuver (CRM): treatment developed for posterior canal BPPV.
Smooth pursuit: eye movements stimulated by a retinal "slip" that generates an error signal to stimulate the oculomotor pathways to keep the visual target on the fovea.
Saccades: rapid eye movements, so fast that you do not see during them, aimed at keeping position of the image on the retina.


Suggested Readings

Brain Injury Association of America - an excellent reference to look to for information on concussions.
http://www.biausa.org/mild-brain-injury.htm

American Psychological Association - discusses more cognitive-related symptoms and the field of Neuropsychology.
http://www.apa.org/helpcenter/concussions.aspx

American College of Sports Medicine - some information regarding sport-related concussions.
https://www.acsm.org/docs/brochures/concussion-in-sports.pdf

Neuroscience News - website containing a section on concussions that is constantly adding new articles.
http://neurosciencenews.com/neuroscience-terms/concussions/


Quiz Questions

Questions

1. What are the three most common vestibular-associated symptoms post-concussion? List one possible underlying mechanism for each.
2. True/False: The cupulolithiasis theory for BPPV attributes symptoms of vertigo to free-floating otolithic debris causing false ampulla stimulation.
3. Which eye movement maintains a stable gaze during head movements?
a. Smooth pursuit
b. Saccades
c. Vestibulo-ocular reflex
4. True/False: The vestibular nuclei are located within the cerebellum.
5. What do the vestibulospinal tracts control, and what is the vestibular systems role in this control?
6. What vestibular structures are located in the labyrinth?
7. Choose the correct order for head-eye coordination exercise progression:
a. Patient follows a target in their visual field and/or switches focus between two targets (standing)
b. Patient maintains a fixed target in their visual field while moving their head (sitting)
c. Patient follows a target in their visual field and/or switches focus between two targets (sitting)
d. Patient follows a target in their visual field and/or switches focus between two targets (walking)
8. True/False: Balancing with eyes closed is one way to strengthen vestibular inputs for control of posture.
9. Which canal is the most commonly affected in BPPV?

Answers

1. Dizziness, impaired vision, and postural instability. Possible mechanisms are BPPV for dizziness, and inaccurate afferent inputs for both vision and postural impairments.
2. False
3. c
4. False
5. Through input regarding head and body position from the vestibular system, the tracts innervate axial muscles for maintenance of posture.
6. The horizontal, posterior and superior semicircular canals, the saccule and utricle, and the vestibular nerve/Scarpa's ganglion.
7. c, b, a, d
8. True
9. The posterior semicircular canal.


References

Aligene, K., & Lin, E. (2013). Vestibular and balance treatment of the concussed athlete. Neurorehabilitation, 32(3), 543-553. doi:10.3233/NRE-130876
Baloh, R., & Honrubia, V. (2001). Clinical Neurophysiology of the Vestibular System (3rd ed.). New York: Oxford University Press.
Cohen, H. (1999). Neuroscience for Rehabilitation (2nd ed.). Philadelphia: Lippincott.
Evans, R. W. (2006). Neurology and Trauma. New York: Oxford University Press.
Furman, J., & Cass, S. (2003). Vestibular Disorders: A Case-Study Approach (2nd ed.). Oxford: Oxford University Press.
Gray, L. (1997-present). Vestibular System: Structure and Function [Online]. The University of Texas Health Science Center at Houston. http://neuroscience.uth.tmc.edu/s2/chapter10.html
Gurley, J. M., Hujsak, B. D., & Kelly, J. L. (2013). Vestibular rehabilitation following mild traumatic brain injury. Neurorehabilitation, 32(3), 519-528. doi:10.3233/NRE-130874
Herdman, S. (2007). Vestibular Rehabilitation (3rd ed.). Philadelphia: F.A. Davis.
Latash, M. (1998). Neurophysiological Basis of Movement. Champaign, IL: Human Kinetics.