Dizziness is a rare complaint among children. In this article, the authors present the embryology and development of the vestibular system, and offer a rational approach to taking a careful history and ordering and interpreting appropriate vestibular and balance testing in children. A differential diagnosis is presented, so that the likely cause of the balance disorder can be elucidated even in the most complex pediatric patients.
Pediatric vestibular disorders are just beginning to be adequately recognized as an area of significant importance in the overall well-being of children. Mandates for universal newborn hearing screening have resulted in an early focus on auditory function in infants, facilitating early identification and management of children with auditory pathology. This approach has vastly improved outcomes for children and has resulted in a welcome increase in awareness that auditory and vestibular pathology frequently co-occur.
From the day we are born until we reach old age, we are profoundly reliant on our sense of balance for well-being and survival. Balance relies on complex interactions and central mediation of 3 important senses: vision, vestibular function, and proprioception. Structurally, the sensory systems related to balance are fully developed at birth. From infancy, balance function continues to mature with sequential acquisition of motor milestones for head control, sitting, standing, and walking, and develops thereafter through experiential learning and adaptation until adolescence. Changes in balance function are most rapid and pronounced during infancy and preschool years when motor milestones needed for walking are realized, and as postural control and coordinated movements are refined. Nevertheless, changes in balance function continue to be evident as a function of aging throughout the human life span.
Overview of the vestibular system
The vestibular system includes 2 otolith organs (the saccule and utricle), which sense linear acceleration (ie, gravity and translational movements), and 3 semicircular canals, orthogonal with respect to each other, which are responsive to angular acceleration. Sensory hair cells are located in the maculae of the otolith organs, and in the ampullae of the semicircular canals. Hair cell activation resulting from endolymphatic fluid flow generates afferent impulses that are transmitted to bipolar cells of the vestibular nerve, whose cell bodies are located in the vestibular ganglia. The axons of bipolar cells pass through the internal auditory canal and reach the medulla, alongside the cochlear nerve. In the internal auditory canal, vestibular fibers are segregated into 2 distinct bundles forming superior and inferior branches of the nerve. The superior vestibular nerve supplies the superior and lateral semicircular canals as well as the utricle. The inferior vestibular nerve supplies the posterior canal and the saccule. The superior and inferior vestibular nerves join to form a common bundle, which enters the brainstem. These first-order neurons terminate in the vestibular nuclei in the floor of the fourth ventricle and do not cross the midline. The 4 major vestibular nuclei include the superior (or Bechterew), lateral (or Deiter), medial, and inferior (or descending) vestibular nuclei. From the vestibular nuclei, projections go to the cerebellum, motor nuclei of the extraocular muscles, antigravity muscles, and contralateral vestibular nuclei. The cortical representation of the vestibular system is at the level of the parietal and insular regions of the cortex.
Embryology
Inner Ear
Ongoing research and technological advances have significantly improved our understanding of the cellular differentiation and morphogenesis of the human vestibular labyrinth. The first stages of inner ear development begin as diffuse thickenings of surface ectoderm on either side of the embryonic (rhomboencephalon) hindbrain. During the third week of embryonic development, thickened surface ectoderm of the embryonic hindbrain begins to invaginate, forming the otic placodes.
During week 4, the otic placodes are surrounded by proliferating embryonic mesoderm, creating otic pits. The otic pits subsequently pinch off from the surface ectoderm to form the closed, rounded structures of the otic vesicles. The otic vesicles further differentiate into upper and lower portions, forming the vestibular apparatus and membranous cochlea, respectively. Different rates of growth among the canals, the vestibular aqueduct, the oval window, the round window, and the cochlea have been observed, which suggests that each part of the inner ear follows distinct trajectories during development. The vestibular apparatus, located superiorly in relation to the cochlea, develops earlier and grows at a faster rate than the cochlea. The otic vesicle elongates and differentiates to form a dorsal utricular portion and a ventral saccular portion. The utricular portion becomes the semicircular canals and the utricle. The superior semicircular canal forms first, followed by the posterior, then lateral canal. The saccular portion becomes the saccule and the cochlear duct. The communication between the saccule and membranous cochlea narrows to form the ductus reuniens.
The bony capsule that surrounds the membranous labyrinth forms rapidly from embryonic mesoderm over a period of approximately 5 weeks, between gestational weeks 19 and 23. Ossification of the otic capsule first occurs in the area of the cochlea and superior semicircular canal at approximately 19 weeks’ gestation. Development appears to progress in an outward fashion from the areas surrounding the vestibule to the canal vertices, with the last area of encapsulation being the posterolateral area of the horizontal semicircular canal at approximately 21 to 23 weeks’ gestation. Current consensus is that the vestibule is adult-like in form and size by 25 weeks of gestation; however, recent findings suggest that some parts of the labyrinth reach final size only after birth. This seems to be the case for the internal aperture of the vestibular aqueduct, which is still growing and is smaller than adult size at 39 weeks.
Maturation of Vestibular Receptors
Around the third week of gestation, sensory epithelia emerge from ectoderm in the cristae forming the semicircular canals, and in the maculae forming the otolith organs. By 7 weeks’ gestation, small quantities of otoconia are present in the utricle. Thereafter, development proceeds quite rapidly, and within 1 week, greater amounts of otoconia are present in both the utricle and saccule, and cellular differentiation of the macular neural substrate is readily evident. At 7 to 12 weeks’ gestation, the calcium content of the otoconia increases markedly in both the utricle and saccule; however, comparisons along the entire continuum of macular development reveal that the otoconia of the utricle appear to be more mature and varied in size and shape than saccular otoconia. Vestibular hair cells first appear at approximately 7 weeks’ gestation. Although not fully differentiated, the beginning of synapse formation in vestibular hair cells is observed in the human fetus at approximately 9 to 10 weeks’ gestation. Differentiation of Type I and Type II hair cells begins between 11 and 13 weeks’ gestation. In general, the morphologic sequence is from apex to base in the cristae and from the center to periphery in the maculae. Significant numbers of fully formed calyx nerve endings are observed at 20 weeks’ gestation. The maturing ampullary cristae become active as early as the eighth or ninth week of fetal life. Vestibular receptors become active by the 32nd week, at which time a fully developed Moro reflex can be elicited. These observations suggest that vestibular afferents are mature and functional in early stages of human development.
Development of Vestibular Pathways
Vestibular ganglion cells are of various shapes until the 21st week of gestation and become uniform in shape around the 24th week of gestation when the development of the inner ear is complete. Morphometric studies show that ganglion cells grow until the 39th week, reaching maturity around the time of birth. Neuronal connections between the labyrinths and the oculomotor nuclei in the brainstem occur between the 12th and 24th weeks of gestation. Myelination of the vestibular nerve begins around the 20th fetal week; it is the first cranial nerve to complete myelination. The vestibular nuclear complex is functional at 21 weeks’ gestation.
Embryology
Inner Ear
Ongoing research and technological advances have significantly improved our understanding of the cellular differentiation and morphogenesis of the human vestibular labyrinth. The first stages of inner ear development begin as diffuse thickenings of surface ectoderm on either side of the embryonic (rhomboencephalon) hindbrain. During the third week of embryonic development, thickened surface ectoderm of the embryonic hindbrain begins to invaginate, forming the otic placodes.
During week 4, the otic placodes are surrounded by proliferating embryonic mesoderm, creating otic pits. The otic pits subsequently pinch off from the surface ectoderm to form the closed, rounded structures of the otic vesicles. The otic vesicles further differentiate into upper and lower portions, forming the vestibular apparatus and membranous cochlea, respectively. Different rates of growth among the canals, the vestibular aqueduct, the oval window, the round window, and the cochlea have been observed, which suggests that each part of the inner ear follows distinct trajectories during development. The vestibular apparatus, located superiorly in relation to the cochlea, develops earlier and grows at a faster rate than the cochlea. The otic vesicle elongates and differentiates to form a dorsal utricular portion and a ventral saccular portion. The utricular portion becomes the semicircular canals and the utricle. The superior semicircular canal forms first, followed by the posterior, then lateral canal. The saccular portion becomes the saccule and the cochlear duct. The communication between the saccule and membranous cochlea narrows to form the ductus reuniens.
The bony capsule that surrounds the membranous labyrinth forms rapidly from embryonic mesoderm over a period of approximately 5 weeks, between gestational weeks 19 and 23. Ossification of the otic capsule first occurs in the area of the cochlea and superior semicircular canal at approximately 19 weeks’ gestation. Development appears to progress in an outward fashion from the areas surrounding the vestibule to the canal vertices, with the last area of encapsulation being the posterolateral area of the horizontal semicircular canal at approximately 21 to 23 weeks’ gestation. Current consensus is that the vestibule is adult-like in form and size by 25 weeks of gestation; however, recent findings suggest that some parts of the labyrinth reach final size only after birth. This seems to be the case for the internal aperture of the vestibular aqueduct, which is still growing and is smaller than adult size at 39 weeks.
Maturation of Vestibular Receptors
Around the third week of gestation, sensory epithelia emerge from ectoderm in the cristae forming the semicircular canals, and in the maculae forming the otolith organs. By 7 weeks’ gestation, small quantities of otoconia are present in the utricle. Thereafter, development proceeds quite rapidly, and within 1 week, greater amounts of otoconia are present in both the utricle and saccule, and cellular differentiation of the macular neural substrate is readily evident. At 7 to 12 weeks’ gestation, the calcium content of the otoconia increases markedly in both the utricle and saccule; however, comparisons along the entire continuum of macular development reveal that the otoconia of the utricle appear to be more mature and varied in size and shape than saccular otoconia. Vestibular hair cells first appear at approximately 7 weeks’ gestation. Although not fully differentiated, the beginning of synapse formation in vestibular hair cells is observed in the human fetus at approximately 9 to 10 weeks’ gestation. Differentiation of Type I and Type II hair cells begins between 11 and 13 weeks’ gestation. In general, the morphologic sequence is from apex to base in the cristae and from the center to periphery in the maculae. Significant numbers of fully formed calyx nerve endings are observed at 20 weeks’ gestation. The maturing ampullary cristae become active as early as the eighth or ninth week of fetal life. Vestibular receptors become active by the 32nd week, at which time a fully developed Moro reflex can be elicited. These observations suggest that vestibular afferents are mature and functional in early stages of human development.
Development of Vestibular Pathways
Vestibular ganglion cells are of various shapes until the 21st week of gestation and become uniform in shape around the 24th week of gestation when the development of the inner ear is complete. Morphometric studies show that ganglion cells grow until the 39th week, reaching maturity around the time of birth. Neuronal connections between the labyrinths and the oculomotor nuclei in the brainstem occur between the 12th and 24th weeks of gestation. Myelination of the vestibular nerve begins around the 20th fetal week; it is the first cranial nerve to complete myelination. The vestibular nuclear complex is functional at 21 weeks’ gestation.
Developmental reflexes
With maturation of physiologic processes and anatomic structures, certain developmental reflexes can be elicited at birth or soon thereafter. These reflexes are primitive in nature, usually disappear as the child matures, and primarily reflect the integrity of the brainstem and spinal cord. Their persistence beyond the normally expected age of dissipation indicates delayed maturation or impaired nervous system function. Their asymmetry suggests either a central or a peripheral nervous system disorder.
The Moro reflex is elicited by holding the child supine and allowing the head to drop approximately 30° in relation to the trunk. Extension and abduction of the arms with fanning out of the fingers followed by adduction of the arms at the shoulder takes place as a normal response. This reflex normally disappears by the age of 5 to 6 months.
The tonic neck reflex is tested by turning the head of the child to one side while supine with the shoulders fixed. The arm and leg of the side toward which the head is turned will extend, while the arm and leg on the opposite side will flex. This reflex normally disappears by the age of 6 months.
The head righting reflex develops by the age of 4 to 6 months. To test this reflex, when the child’s trunk is held 30° from vertical, a normally responding infant will tilt the head so as to remain vertical. At about age 5 months, the child will additionally move the lower limbs away from the side to which they have been tilted, thereby reflecting functional integration of visual, vestibular, and proprioceptive stimuli.
The parachute reaction is elicited beyond the age of 5 months, when a sudden downward movement of a vertically held child causes the lower limbs to extend and abduct. This reflex is considered to represent visual-vestibular interaction with the otoliths presumably involved.
The doll’s eye response is found normally in full-term babies within 2 weeks of birth. When the baby (facing the examiner) is held at arm’s length and rotated in one direction around the examiner, a deviation of the eyes and head opposite to the direction of the rotation is produced, representing vestibular activity. Due to an immature saccadic system at this stage, the fast component of a normal nystagmic response is not seen. Later, however, nystagmus is apparent with the fast component in the direction of rotation.
Development of vestibular-induced reflexes
Balance and equilibrium are maintained through a series of events triggered by sensory stimulation. Incoming sensory inputs received from the vestibular, visual, and somatosensory/proprioceptive systems are directed to the vestibular nuclei and cerebellum for processing and calibration. In response to afferent inputs, the vestibular nuclear complex creates direct and remarkably rapid efferent connections to muscles controlling the eyes, the neck, and the spinal cord. These motor outputs result in 3 categories of vestibular reflexes (vestibulo-ocular, vestibulospinal, and vestibulocollic), which allow us to maintain our balance and equilibrium. It is through examination of these reflexes that we are provided a window for uncovering vestibular dysfunction. Understanding how vestibular responses differ among infants, children, adolescents, and adults is crucial when attempting to evaluate and diagnose vestibular pathology.
Vestibulo-Ocular Reflex
The purpose of the vestibulo-ocular reflex (VOR) is to stabilize gaze and maintain clear vision when the body or head is in motion. Objects of visual interest are maintained on the fovea of the retina through inputs from the semicircular canals and otolith organs.
Data regarding VOR function in infants and children have been somewhat limited historically, due to technical difficulties inherent in achieving compliance and obtaining accurate recordings. The VOR is subject to alteration from a variety of nonvestibular influences, including subject attention and state of arousal, unintended ocular fixation due to light leaks, inadequate calibration, and insufficient head stabilization during testing. In several decades of research with children, a variety of techniques have been employed to explore and record the pediatric VOR (see article by the Valente in this publication). These methods include caloric stimulation, rotational stimulation (torsion swing), as well as passive whole body (en bloc) rotation techniques. Depending on the technique employed, parameters such as speed of the slow component in degrees of eye movement per second, amplitude of nystagmus beat, as well as latency and duration of response have been recorded. Researchers using en bloc rotation techniques have explored factors such as gain (ratio of peak eye velocity to peak head velocity), phase (timing difference between head and eye velocities), symmetry (comparison of rightward and leftward eye velocities), and time constant of decay (time for the slow-phase eye velocity to decline by two-thirds of its maximum value).
The VOR is present at birth; however, its time constants are found to be approximately one-half of normal adult values in neonates aged 24 to 120 hours. Time constants appear to approach adult values by 2 months of age. These differences are likely a reflection of immaturity of the visual pathways at birth, which suggests that maturation of the visual pathways is a necessary precursor for adequate calibration of the VOR and for competent function of the velocity storage mechanism necessary for stable vision. Reflexive slow component nystagmus of the VOR generated by vestibular stimulation is routinely observed at birth. However, the centrally mediated fast component, which returns and maintains the eyes within the physical confines of the orbits, is variably present. Infants demonstrate inaccurate saccades, frequently requiring more than one saccade to reach the target. The saccadic system is immature at birth, continuing to develop up to the age of 2 years. The speed of the slow component as well as the frequency of beats increase as a function of age until age 6 to 12 months, after which values reach a plateau and stabilize. Smooth pursuit is also only possible at very low frequencies in this age group, due to foveal immaturity. A higher gain of the VOR response to sinusoidal rotation is observed in children compared to adults, and poorer suppression of the VOR response is seen due to immature visual-vestibular interaction. Gain and time constant parameters of the VOR in response to constant angular acceleration reveal that time constants increase, whereas VOR gain shows small but significant decreases as a function of age from 2 months to 11 years of age. In a recent large longitudinal study, Casselbrant and colleagues observed that in response to both sinusoidal and constant velocity rotations on an earth vertical axis, VOR gain increases linearly as a function of age from 3 to 9 years, although phase differences appeared to remain stable. These findings are in contrast to several other studies that have shown decreasing or stable VOR gain as a function of a child’s increasing age.
In summary, the VOR goes through several developmental stages, with healthy responses developing by several months beyond full term. Absence of the VOR by the age of 10 months should be considered an abnormal finding. It is evident that regardless of the parameters explored, the prevailing constant across all studies of the pediatric VOR is that qualitative differences exist between the VOR functions of children and adults, and that these differences seem to persist until pre-adolescence.
Vestibulospinal Reflex
Whether the body is stationary or in motion, continuous afferent signals from vision and vestibular inputs detect the body’s orientation and relationship to gravity. These inputs combine with touch receptors on the skin as well as proprioceptors on the soles of the feet, the hands, joints, and torso to detect the body’s contact with the environment. The sum of these inputs provides the information needed to generate the vestibulospinal reflex (VSR), which stabilizes the body and maintains postural control. VSR output signals travel along 3 major pathways, including the lateral, medial, and reticulospinal tracts. When activated, these tracts impact anterior horn cells of the spinal cord and generate myotatic deep tendon reflexes in the antigravity skeletal muscles of the limbs and trunk.
The VSR has more numerous and complex innervations than the VOR, but just as the VOR works to contract and relax paired ocular muscles, the VSR works similarly to create push-pull arrangements of agonist and antagonist muscle firing across the neural axis. A variety of diagnostic tests exploring aspects of VSR function have been developed for use with both children and adults. In general, when comparing the VSR function of children with adults, as noted by Rine, the postural control of these groups varies significantly. As detailed later in this article, the vestibulospinal mechanism or effectiveness of the vestibular system in postural control continues to develop until at least 15 years of age.
Vestibulocollic Reflex
The vestibulocollic reflex (VCR) plays an important role in stabilizing vision by compensating for head movements when the body is in motion. Through patterned contractions of the neck muscles, the VCR minimizes bobbing of the head caused by vibrations transmitted from the heels as they strike the ground during walking and running. Thus, the VCR assists in stabilizing the head on the neck and in keeping the head still and level, especially during ambulation. During walking, vestibular signals caused by linear translations stimulate nerve receptors of the saccule. In response, the saccule transmits afferent signals along the inferior vestibular nerve and ganglion to the vestibular nuclear complex in the brainstem. From the vestibular nucleus, efferent signals are sent via the medial vestibulospinal tract and spinal accessory nerve to the neck muscles, including the sternocleidomastoid muscles—one of the long neck muscles extending from the thorax to the base of the skull behind the ear.
In the last decade, VCR function has become routinely evaluated through recordings of vestibular evoked myogenic potentials (VEMPs). VEMPs have become an increasingly popular clinical technique because, unlike other tests of vestibular function, information is provided regarding saccular and inferior vestibular nerve function. This is a significant benefit, because the otolith organs and superior and posterior semicircular canals may be more instrumental in locomotion and posture control than the horizontal semicircular canals, evaluated using the VOR. In addition, the VEMP test is an objective measure that can be reliably recorded from surface electrodes in a wide variety of patients, including infants and young children. VEMPs are stimulated by high-intensity auditory stimuli that cause robust vibration of the ossicular chain and stimulate the saccule, resting in close proximity. Impulses traveling along the VEMP neural pathway stimulate the VCR, creating an efferent inhibitory release of the tonically contracted sternocleidomastoid muscle. VEMP recordings appear as biphasic electromyographic potentials, with an initial positive deflection at 13 milliseconds post stimulus onset (P13), and a negative deflection at 23 milliseconds (N23).
Studies recording VEMPs in preterm neonates, infants, and young children have confirmed the presence of VEMP responses in the pediatric population. These studies have pointed out differences between the VEMP responses of children and adults, suggesting maturational effects from preschool age through adolescence.
Balance and motor development
Maintenance of postural balance requires an active sensorimotor control system. In adults, the sensory systems are well organized and act in a context-specific way. Postural control involves sensory feedback, and visual and proprioceptive inputs need to be integrated in order for the center of foot pressure to move in phase with the center of mass. In children the sensory systems are not completely developed, although their anatomic structures are mature early in life. The proprioceptive, visual, and vestibular systems develop more slowly than automatic motor processes that mature early in childhood. The importance of visual cues in maintaining static posture has been well demonstrated, particularly in children who are used to visually monitoring the body during posture. Also important are cognitive functions for organization and integration of available sensory information, in both static and dynamic conditions, and this also has been well documented. Hence, the selection of the appropriate balance strategy not only depends on environmental demands but is also a function of central nervous system maturation and experience.
In typically developing children, the growth of postural stability proceeds in a cephalocaudal fashion, with the infant achieving control of the head first, then the trunk, and finally postural stability in standing. The newborn infant when held ventrally with a hand under the abdomen cannot hold up the head. By 6 weeks of age the head is held in the plane of the body, and above this level by 12 weeks. Head control allowing the baby to look around in a horizontal plane is achieved by 16 weeks of age, and by the 36th week, the infant is able to sit unsupported for a few minutes. By the age of 1 year the child is able to crawl on hands and knees, and stand up holding on to furniture. At about 15 to 16 months of age the child is able to start walking.
The coordination of postural responses develops until at least 10 to 15 years of age. In balance control, somatosensory inputs are given priority in adults, whereas children prefer visual inputs to vestibular information in achieving postural equilibrium. Infants and young children (aged 4 months to 2 years) are dependent on the visual system to maintain balance. At 3 to 6 years of age, children begin to use somatosensory information appropriately, although some studies indicate that development continues until the age of 9 to 11 years. In the case of intersensory conflict, the vestibular system acts as a referential function by suppressing input not congruent with vestibular information. Adults may improve their postural control, even with misleading visual information, due to presumed mature vestibular function, whereas children by age 12 are still not able to select and process misleading visual information. Among the 3 sensory inputs in children, the vestibular system seems to be the least effective in postural control, and functional efficiency of the vestibular system in children 10 to 15 years old is still developing. The ultimate development of several visual functions (eg, saccade latency, contrast sensitivity, and chromatic sensitivity) does not asymptote to adult level until about 12 years of age. The visual influence on standing stability is reported to be established at adult levels around the same age of 15 years. Adult-like postural stability due to complete maturation of the 3 sensory systems and the ability to resolve intersensory conflict situations can thus be assumed in adolescents around 15 years of age.
In summary, vestibular function is present at birth, but continues to mature so that it is most responsive between 6 and 12 months of age. Subsequently, vestibular responses are gradually modulated by developing central inhibitory influences, cerebellar control, and central vestibular adaptation, and reach adult-like values around 15 years of age.
Incidence of vestibular disorders in the pediatric population
The general prevalence of pediatric vestibular dysfunction is estimated at between 8% and 18%, though the incidence of vertigo as a primary complaint in a review of hospital records was less than 1%.
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