--------------------------------------------------------------------------------
 TITLE:   VESTIBULAR ANATOMY AND PHYSIOLOGY
 SOURCE:  Dept. of Otolaryngology, UTMB, Grand Rounds
 DATE:    December 9, 1992
 RESIDENT PHYSICIAN:     Robert Hoffman, MD
 FACULTY:                Chester Strunk, MD
 DATABASE ADMINISTRATOR: Melinda McCracken, M.S.
--------------------------------------------------------------------------------

 "This material was prepared by resident physicians in partial fulfillment 
 of educational requirements established for the Postgraduate Training 
 Program of the UTMB Department of Otolaryngology/Head and Neck Surgery 
 and was not intended for clinical use in its present form.  It was 
 prepared for the purpose of stimulating group discussion in a conference 
 setting.  No warranties, either express or implied, are made with respect 
 to its accuracy, completeness, or timeliness.  The material does not 
 necessarily reflect the current or past opinions of members of the UTMB 
 faculty and should not be used for purposes of diagnosis or treatment 
 without consulting appropriate literature sources and informed 
 professional opinion." 
 
 
 VESTIBULAR ANATOMY AND PHYSIOLOGY
 
 
 I. Introduction

 The vestibular system is the system of balance.  In simple
 term it consists of five distinct end organs: three
 semicircular canals that are sensitive to angular
 accelerations and two otoliths that are sensitive to linear
 accelerations.  The semicircular canals are arranged at right
 angles to the other two in the set much the way the three
 sides of a box that meet at each corner are at right angles to
 one another.  Each canal is maximally sensitive to rotations
 that lie in the plane of that canal.  The canals are also
 organized into functional pairs wherein both members of the
 pair lie in the same plane.  Any rotation in that plane will
 be excitatory to one of the members of the pair and inhibitory
 to the other.  The horizontal canals form one obvious pair. 
 For the vertical system, the anterior canal on one side is
 parallel and thus coplanar with the posterior canal on the
 opposite side.  
 
 II. Vestibular End Organs
 
   A. Embryology of vestibular apparatus     

 At about 22 days, the surface ectoderm overlying the
 future site of the inner ear thickens to form the otic
 placode.  This invaginates and forms the otocyst.  This then
 forms the endolymphatic diverticulum from the medial portion
 and the utriculosaccular chamber from the lateral aspect. 
 This chamber then differentiates into an utricular chamber
 that will give rise to the utriculus and the semicircular
 ducts and a saccular chamber that becomes the sacculus and
 the cochlea.  The superior semicircular canal forms first
 from the utricular chamber. This is followed by the
 development of the posterior and lateral ducts.  The
 saccular chamber differentiates as the cochlear duct
 expands.  The duct becomes separated from the sacculus by a
 narrowing of the duct to form the ductus reuniens.  The
 specialized neuroepithelium appears at about the third week. 
 It forms the utricular and saccular macula and cristae
 ampullares of the semicircular ducts.  The hair cells are
 mature by the ninth week.      
 
   B. Relational anatomy

   The vestibular apparatus is enclosed with a bony
 labyrinth, the vestibule, in the petrous portion of the
 temporal bone.  The three semicircular canals are oriented
 in different planes.  The two vertical semicircular canals
 are the anterior (or superior) and posterior canals.  The
 horizontal canal is also known as the lateral canal.  The
 vertical canals are oriented roughly at 45o in relation to
 the sagittal plane, and the horizontal canal is tilted
 upward about 30o anteriorly from the horizontal plane.  The
 two macula are oriented in approximately 90o planes.  The
 utriculus is in the horizontal plane and the sacculus in
 oriented in the vertical plane.  
   The vestibule is situated between the internal auditory
 meatus anteromedially and the middle ear cavity laterally. 
 The entrance to the mastoid antrum is just lateral to the
 horizontal semicircular canal.  The cochlea sits anterior to
 the vestibule and is connected to the vestibule by the
 narrow ductus reuniens.  Posterior and lateral to the
 vestibule are the mastoid air cells.  Directly medial is the
 posterior cranial fossa, into which the endolymphatic duct
 and sac extend beneath the dura.  The seventh and eighth
 cranial nerves enter the vestibule and cochlea from the
 internal auditory meatus located medial to a point midway
 between the cochlea and vestibule.  The facial nerve lies
 anterior and dorsal to the vestibulocochlear nerve.  The
 vestibulocochlear nerve splits into a vestibular division,
 which turns posteriorly to supply the vestibule and a
 cochlear division, which turns anteriorly to supply the
 cochlea.  The vestibular ganglion sits at the bottom of the
 internal auditory meatus.  It has two parts, the superior
 vestibular ganglion and the inferior vestibular ganglion. 
 The superior (or anterior) vestibular nerve supplies the
 anterior and horizontal cristae and the utricular macula. 
 The inferior (or posterior) vestibular nerve supplies the
 posterior canal and saccular macula.  
 
   C. Blood Supply

   The main blood supply to the vestibular end organs is
 through the internal auditory (labyrinthine) artery, which
 arises most often (45%) from the anterior cerebellar artery,
 superior cerebellar artery (24%) or basilar artery (16%). 
 The labyrinthine artery divides into two branches: the
 anterior vestibular artery and the common cochlear artery. 
 The anterior vestibular artery provides the blood supply to
 most of the utriculus and the superior and horizontal
 ampullae, as well as some blood to a small portion of the
 sacculus.  The common cochlear artery forms two divisions,
 the proper cochlear artery and the vestibulocochlear artery. 
 The latter then divides into a cochlear ramus and the
 posterior vestibular artery.  This is the source of blood
 supply to the posterior ampulla, the major part of the
 sacculus, and parts of the body of the utriculus and
 horizontal and superior ampullae.
 
 III. Endolymph and Perilymph
 
   A. Endolymph

   The five vestibular end organs, along with the cochlea,
 are contained with in an endolymph filled membranous
 labyrinth (the endolymphatic space), which is it self
 contained in the perilymph filled bony labyrinth (the
 perilymphatic space).  Endolymph has a low Na+ content and a
 high K+ content causing it to resemble intracellular rather
 than extracellular fluid.  It is produced by the marginal
 cells of the stria vascularis as a derivative of perilymph. 
 The site of absorption of endolymph is presumed to be the
 endolymphatic sac, which is connected to the utriculus and
 sacculus by means of the endolymphatic duct and utricular
 and saccular ducts.  Experimental blockage of the
 endolymphatic duct produces endolymphatic hydrops,
 supporting this as the site of absorption.  The ionic
 concentrations in endolymph are as follows: K+ = 144 mEq/L,
 Na+ = 5 mEq/L, Protein = 126 mg%.
 
   B. Perilymph

 The site of perilymph production is still controversial.  It
 is unclear whether perilymph is derived as an ultrafiltrate
 of blood or from CSF.  CSF can reach the vestibule by means
 of the vestibular aqueduct or by means of perivascular and
 perineural channels.  But because of its chemical
 composition, there is more evidence that perilymph is an
 ultrafiltrate from blood.  Perilymph leaves the ear by
 drainage through venules and through the middle ear mucosa. 
 The ionic concentrations in perilymph are as follows: K+ =
 10 mEq/L, Na+ = 140 mEq/L, Protein = 200 to 400 mg%. 
 
 IV. Anatomy of Vestibular End Organs
 
   A. The Ampulla

   At the dilated end of each semicircular duct is the
 ampulla.  It contains the neuroepithelium (crista
 ampullaris), the cupula, supporting cells, connective
 tissue, blood vessels, and nerve fibers.  The crista is a
 saddle shaped, raised section of the wall that extends
 across the floor of the ampulla at right angles to its long
 axis.  The crista has been found to divided into central and
 peripheral zones based on the morphology and physiology of
 vestibular afferents supplying the different regions.  The
 shape of the crista facilitates maximal packing of
 specialized mechanoreceptor hair cells.  Both the hair cells
 and the supporting cells are modified columnar epithelial
 cells that have microvilli on their apical surfaces.  In the
 hair cells, many of these microvilli are elongated to form
 stereocilia, which are grouped in an organ pipe-like
 arrangement.  In addition, each hair cell has a single long
 kinocilium, a true cilium demonstrating the 9+2 arrangement
 of microtubules.  This kinocilium is longer than the
 stereocilia and eccentrically located, imparting a certain
 polarization to the hair cell that has important functional
 implications.  Displacement of the stereocilia bundle toward
 the kinocilium results in an increase in the firing rate of
 the afferent fibers contacting the hair cell.  Displacement
 of the hair bundle away from the kinocilium results in a
 decrease in firing rate.  In the cristae the kinocilium on
 each hair cell is located on one end of the cell.  In the
 horizontal crista the kinocilia are located on the side of
 the hair cell that is closest to the utriculus.  In the
 vertical cristae the kinocilia are located on the side of
 the hair cell furthest from the utriculus, the canalicular
 side.  The entire hair bundle extends upward into the
 cupula.
   The cupula is a gelatinous mass of mucopolysaccharides
 within a keratin meshwork.  It extends from the surface of
 the cristae to the roof and lateral walls of the membranous
 labyrinth, forming a fluid tight partition.  There is a
 distinct subcupular space in the region of the cupula
 overlying the apex of the center of the crista.  This
 subcupular space is believed to provide space for freedom of
 movement and more sensitive responses to endolymph flow for
 the stereocilia on the hair cells in the central zone.  The
 specific gravity of the cupula is approximately 1.0 which is
 about the same as that of the endolymph.  This matching of
 the specific gravity of the cupula and the endolymph is
 necessary to prevent the cupula from "floating up"  in
 certain head positions and causing an enduring nystagmus. 
 Disruption of this match in specific gravity is likely the
 cause of postalcoholic nystagmus.
 
   B. The Macula

   The macula of the utriculus and sacculus consist of
 neuroepithelium, supporting cells, blood vessels, and nerve
 fibers.  The utricular macula is oriented in the horizontal
 plane, and the saccular macula is oriented in the vertical
 plane.  Cilia from the hair cells in both maculae extend
 upward into their respective otolithic membranes, gelatinous
 membranes somewhat analogous to the cupula.  In the upper
 surface of the otolithic membranes, the otoliths (or
 otoconia) are embedded.  Otoliths are inorganic crystalline
 deposits composed of calcium carbonate or calcite.  They
 vary in size from 0.5 to 30 um, with most being about 5 to 7
 um.  The specific gravity of the otolithic membrane is much
 higher than that of the endolymph, about 2.71 to 2.94. 
 Within the otolithic membrane is the striola, a specialized
 central region that has a snowdrift-like appearance.  The
 striola is identifiable as a thin stripe running down the
 center of the otolith membranes of both maculae.  In the
 striola the otoliths are very small and the thickness of the
 otolithic membranes is either reduced, as in the utricular
 macula, or increased, as in the saccular macula.  These
 regional differences in the otolithic membranes are
 paralleled by morphologic and physiologic differences in the
 afferent fibers supplying the hair cells in the underlying
 sensory epithelium.
   The kinocilia on the hair cells in the maculae are also
 dynamically polarized, but the pattern of polarization is
 much more complex than in the cristae.  In the utricular
 ampulla, the kinocilia are oriented so that they point
 toward the striola, whereas in the saccular macula, the
 kinocilia point away from the striola.  However, since both
 maculae are curved areas and the striolae therefore are
 curved lines, the arrangement is so complex that static head
 tilts in any direction cause some hair cells to be excited
 and others to be inhibited in one or both of the otolithic
 organs.  Thus the stimulus is encoded by means of
 stimulation of hair cells in the appropriate sector of the
 macula.  The otolith organs are sensitive not only to
 gravity but also to other linear acceleration forces, such
 as forward motion and bobbing movements of the head during
 walking.  Thus static head tilts are represented by a vector
 and the afferent response predicted by a trigonometric
 function based on this simple relation; however, there is a
 response asymmetry in that the excitatory response is
 somewhat larger than the inhibitory response.  As a
 consequence, the equation describing this force response
 relation is by necessity nonlinear.                          
                    .
 V. Cellular Morphology of Vestibular Sensory Epithelium
 
   The sensory epithelium is make up of several different
 elements: hair cells, supporting cells, afferent nerve fibers
 and their synaptic terminals, and efferent nerve fibers and
 their synaptic boutons.  
   Two basic cell types are present within the sensory
 epithelium: supporting cells and hair cells.  Supporting cells
 extend from the basement membrane to the apical surface. 
 Their nuclei are usually found just above the basement
 membrane and below the hair cells.  In sections taken
 tangential to the apical surface, several supporting cells can
 be seen to form a ring around an individual hair cell.  The
 supporting cells themselves contain well developed Golgi
 complexes, many mitochondria, and occasional lipid droplets. 
 The upper part  of the supporting cells contains large numbers
 of round or ovoid granules.  The function of these secretory
 granules is uncertain, but it is conceivable that they may be
 responsible for the formation of the cupula and otolithic
 membrane. 
   Hair cells, in general, contain a bundle of stereocilia
 attached to their apical surface and grouped in a staircase
 arrangement.  These stereocilia are densely packed with
 longitudinally oriented actin filaments that extend into the
 hair cell and are anchored in a thickened region near the
 apical surface, termed the cuticular plate.  The cuticular
 plate is a dense filamentous meshwork of randomly oriented
 actin filaments that fills up the area just under the apical
 surface of the cell, except for the region of the kinocilium. 
 In the region of the kinocilium, there are usually a basal
 body and many large vesicles.  Hair cells are surrounded by
 supporting cells, as mentioned above, and form tight junctions
 and desmosomes with the supporting cells, thus separating the
 endolymphatic space, in which endolymph bathes the stereocilia
 above the cells, from the perilymphatic space below the apical
 surface.  Another general feature that applies to hair cells
 is that they are presynaptic to the afferent nerve fibers that
 they contact.  Hair cells make synaptic contacts by means of
 synaptic specializations termed synaptic ribbons or bars,
 electron dense structures with synaptic vesicles clustered
 around them.
 
 VI. Synaptic Morphology of Vestibular Afferents
 
   Hair cells are of two types, type I and type II, defined by
 the presence or absence of a calyx, or chalice, a specialized
 type of large afferent ending that completely surrounds the
 cell except for the near apical and apical surfaces.  Type I
 hair cells are flask shaped cells surrounded by a calyx
 ending.  Usually, a calyx will surround a single type I hair
 cell.  In this case the calyx ending is termed a simple calyx
 ending.  Sometimes one calyx will surround two to four type I
 hair cells.  This is termed a complex calyx ending.  Complex
 calyx endings are much more common in the central zone (or
 striola) than in the periphery.  In fact, histologically, the
 existence of complex endings is a criterion that can be used
 to define the central zone.  The ratio of type I to type II
 hair cells in the central zones may be as high as 5:1. 
   Type II hair cells are cylinder shaped cells that are
 contacted at their basal surfaces by numerous afferent and
 efferent synaptic boutons.  Afferent boutons contain
 mitochondria and few vesicles and receive synaptic contacts
 from the hair cell.  They transmit the impulse centrally to
 the vestibular nuclei and are postsynaptic to the hair cell. 
 Efferent boutons contain many vesicles and smaller
 mitochondria and vesicles than those found in afferent
 boutons.  This form synapses with hair cells and afferents,
 and transmit impulses from the efferent group of neurons
 located in the brain stem.  They are presynaptic to hair
 cells.  It has long been assumed that hair cells from
 different regions had approximately the same number of
 afferent boutons contacting them and that each bouton formed
 about the same number of synapses with a given hair cell. 
 Recent ultrastructural work has shown that there are regional
 variations in the synaptic innervation of type II hair cells. 
 Type II hair cells in the periphery make synaptic contact
 with many afferent boutons, each of which receives one
 synapse from the adjacent hair cell.  Type II hair cells in
 the central zone (or striola) make synaptic contact with
 relatively few afferent boutons but make multiple contacts
 with each of these.  In addition, type II hair cells in the
 central zone make synaptic contacts with the outer surface of
 the calyx endings surrounding type I hair cells, a type of
 synapse that is rarely found in the peripheral zone.   
   
 VII. Synaptic Morphology and Function of Vestibular Afferents
 
   Vestibular afferents endings have also been classified
 into three morphologic types: pure calyx (or chalice)
 endings, bouton endings, and dimorphic endings (which
 contain both calyx and bouton terminals.  The distribution
 of these three types of afferent endings are segregated
 within the sensory epithelium.  Pure calyx endings have a
 very irregular discharge pattern and are fairly insensitive
 in response to sinusoidal head rotation.  Calyx endings were
 found only in the central region.  Bouton  endings are very
 regularly discharging and have low sensitivity to sinusoidal
 head rotation and dimorphic endings can vary from very
 regular to very irregular in discharge rate and from very
 low gain to very high gain response dynamics.  Bouton
 endings are always found near the periphery.  Dimorphic
 endings are found throughout the sensory epithelium, but
 irregular dimorphic endings were found in the central zone
 and regular dimorphic endings were found in the peripheral
 zone.
 
 VIII. Central Vestibular Pathways   
 
   A. Anatomy

    1. Primary Afferent Connections
   The vestibular system functions primarily as an afferent-
 reflex input to the motor system.  In general, vestibular
 pathway mediated reflexes involve three muscular systems:
 extrinsic oculomotor, cervical, and antigravity.
   As might be expected, the semicircular canals (rotational
 sensors) connect primarily with the extrinsic oculomotor
 and cervical muscles (muscles that compensate for head
 rotation), whereas the otolith organs (position sensors)
 connect primarily with the antigravity muscles.  
   Scarpa's ganglion, in the internal auditory canal within
 the vestibular portion of the eighth nerve, contains the
 bipolar ganglion cells of the first order vestibular
 neurons.  The vestibular nerve can be divided into superior
 and inferior divisions that innervate the sensory epithelia
 of the canal and otolithic end organs.  The superior
 portion innervates the cristae of the superior and
 horizontal semicircular canals, the utricular macula, and a
 small region of the saccular macula.  The inferior division
 of the vestibular nerve innervates the crista of the
 posterior semicircular canal and the remaining part of the
 saccular macula.  Centrally, all first order vestibular
 neurons synapse in the vestibular nucleus complex, which
 occupies a considerable area beneath the floor of the
 fourth ventricle and lies across the pontomedullary
 boundary. On entering the brainstem, the vestibular axons
 bifurcate into the ascending rostral and descending caudal
 divisions.
   The vestibular nucleus complex consists of four distinct
 subnuclei: superior, lateral, medial, and inferior nuclei. 
 Each subnucleus has a unique set of connections with the
 periphery and with specific regions of the central nervous
 system including the spinal cord, cerebellum, and brainstem
 oculomotor nuclei.  Most of the semicircular canal
 afferents terminate in the superior nucleus and rostral
 portion of the medial vestibular nucleus.  Both of these
 nuclei in turn project to the oculomotor nuclei of the
 extraocular muscles by way of the ascending MLF.  The
 superior nucleus projects only to the ipsilateral MLF,
 whereas the medial nucleus projects bilaterally.  The
 medial nucleus, by way of the medvestibulospinal tracts in
 the descending MLF, also sends bilateral descending
 projections to spinal anterior horn cells that control the
 cervical musculature.  Thus, the input and output of the
 superior and medial vestibular nuclei provide a possible
 anatomic basis for the nystagmus and head turning reflex
 responses to semicircular canal stimulation.
   The otolith organs project primarily to the inferior
 nucleus and caudal part of the lateral nucleus.  Outputs
 from these nuclei, in turn, project downward to the ventral
 horn region throughout the length of the spinal cord by way
 of the lateral vestibulospinal tract.  Thus, the afferent
 and efferent connections of the lateral vestibular nucleus
 provide a possible anatomic basis for antigravity muscle
 responses in the limbs (extensors of the legs and flexors
 of the arms) to postural change.  The otolith organs have
 relatively sparse connections to the extraocular muscles. 
 These may be the connections that produce the ocular
 counter rolling response to head tilt.
 
   B. Vestibulocerebellar Connections

    1. Primary Vestibular fibers
   Primary vestibular neurons project not only to the
 vestibular nuclei, but also to the cerebellum.  Most of
 these fibers are distributed to the ipsilateral flocculus
 and nodulus and the medially located uvula.  Because of
 this innervation by primary vestibular fibers, these three
 cerebellar areas have been termed collectively the
 vestibulocerebellum.  
    2. Secondary Vestibular Fibers
   The vestibulocerebellum receives secondary fibers
 primarily from the medial and inferior vestibular nuclei,
 but also from the other divisions.  In addition, the
 fastigial nucleus and the cortex of the vermis receives a
 strong, somatotopically organized projection from the
 lateral vestibular nucleus.  Because this nucleus is the
 primary origin of the vestibulospinal tract, connections to
 it from the cerebellum are probably important in regulating
 antigravity reflexes that help to maintain an upright body
 posture.  
 
 IX. Transduction and Coding    
 
   A. Mechanism of stimulation

   Each of the semicircular ducts, with its ampulla and the
 utricle, can be thought of simplistically as a circular,
 fluid filled tube (toroid) of varying diameter (larger at
 the utricle and ampulla) with an internal partition, the
 cupula, across it at one spot.  The pendulum model has been
 used for describing the physiologic properties of the
 semicircular canals and its electromechanical activity.  The
 cupula acts as the coupler between the force associated with
 angular acceleration of the head and the hair cell which
 leads to the production of action potentials in the
 vestibular afferent fibers. Endolymph can move in only one
 direction in the canal.  When an angular acceleration is
 applied to the head, displacement of the cupula-endolymph
 system acting as a solid mass is opposed by three
 restraining forces: (1) an elastic force caused by the
 cupula's springlike properties, (2) the force from the
 cupula-endolymph viscosity, (3) an inertial force caused by
 the fluid's mass.  Cupula displacement is therefore
 determined by the rate of angular acceleration and the three
 restraining forces.
   As in the cochlea, the final mechanical event in
 vestibular transduction is the bending of the hair cell
 cilia.  When the macula surface is tilted, the heavy
 otoliths slide downward, carrying the gelatinous membrane
 and attached cilia with them.  When the head rotates, the
 inertia of the endolymph causes movement relative to the
 canal walls and cupula.  The endolymph pushes the cupula,
 which carries the cilia with it.  The cilia swings like a
 trap door with a "hinge" at the crista surface.
   
   B. Bioelectric Events

   There are several similarities between bioelectric events
 in the vestibular apparatus and in the cochlea.  As in the
 cochlea, there is constant positive voltage level in the
 vestibular endolymphatic space with its boundary at the
 apical ends of the hair cells.  This vestibular "resting
 potential" (about 50mv) is of lesser magnitude than the
 endocochlear potential (80 mV) in the cochlea.  As in the
 cochlea, bending of the vestibular hair cell cilia modulates
 the resting potential to produce a receptor potential. 
 There is a clear relationship between the morphologic
 polarization of the hair cell cilia, the polarity of the
 receptor potential, and neural excitation and inhibition. 
 When the stereocilia are bent toward the kinocilium, the
 resting potential is reduced (partial "depolarization"
 occurs), and the afferent neuron synapsing with the hair
 cell is excited.  The opposite of these effects occurs when
 the stereocilia are bent away from the kinocilium.
   In the horizontal canal, bending the cupula toward the
 utricle (utriculopetal or ampullopetal), so that all
 kinocilia are deflected away from the stereocilia decreases
 the ampullar resting potential (depolarization) and
 increases neural firing rate.  Bending the cupula away from
 the utricle (utriculofugal or ampullofugal) so that all
 kinocilia are deflected toward the stereocilia, increases
 the resting potential (hyperpolarization) and decreases
 neural firing rate.  In the vertical canals, these
 directional effects are exactly opposite.  Thus, the
 opposing morphologic polarization of the vertical and
 horizontal hair cells (vertical canals: kinocilia oriented
 toward the utricle) described previously has the expected
 functional correlate.  The more complex arrangement of
 morphologic polarization in the macula of the utricle and
 saccule implies that all four directions of functional
 polarization are represented in these end organs.  Thus,
 macular receptors may be able to respond to linear
 accelerations in all directions.
 
   C. Response of Primary Vestibular Neurons.

   Microelectrode studies in higher mammals have demonstrated
 the following characteristics of primary vestibular neuron
 activity: most of the primary vestibular neurons called
 regular units have a high (about 100/sec) and remarkably
 uniform spontaneous discharge.  There is also a small
 population of irregular neurons with a lower rate and less
 regular spontaneous discharge.  The high rate regular units
 have small diameter, slowly conducting axons that
 predominantly innervate the periphery of the end organ (type
 II hair cell region of the crista); the low rate irregular
 neurons come from the center of the crista where most type I
 hair cells are located.  The high, regular spontaneous
 firing rate of the primary neurons permits the bidirectional
 sensitivity of the vestibular hair cell receptors.
   When the head rotates (causing cupula displacement and a
 stimulatory deflection of hair cell cilia), the semicircular
 canal afferents change their discharge rate above (in
 response to hair cell depolarization) and below (in response
 to hair cell hyperpolarization) the resting rate depending
 on the direction of rotation.  When the head rotates
 sinusoidally at velocities encountered during normal
 function, ampullar nerve discharge rate varies sinusoidally. 
 The phase relationship between head position and head
 velocity (phase lag of about 90 degrees) is such that the
 maximum discharge rate occurs at the head's zero crossing -
 i.e. at the head's maximum velocity.  Thus, the ampullar
 afferent discharge rate codes head angular velocity.  The
 adequate stimulus is actually angular acceleration, but the
 hydrodynamics of the semicircular canal system are such that
 the head's acceleration is integrated to give a velocity
 output.  
   Similarly, with the macular afferents, accurate coding by
 discharge rate of the head's position relative to
 gravitational vertical can be demonstrated in all species. 
 The more complex orientation of the macular hair cells makes
 directional correlates more difficult to establish than for
 semicircular canal afferents.  However, large populations of
 saccular and utricular neurons and were able to demonstrate
 neural "sensitivity vectors" among the neuronal populations
 that corresponded to the relative orientations of the
 saccular and utricular maculae.
 
 X. Mechanics of Semicircular Canal and Otolith Organ Function 
 
 Such a conceptualization for both the right and left horizontal
 semicircular canals is shown in Figure 1.  
 
 Condition       Left DP      VN     Right DP    CEM   FPN   Fall
 
 Head           | | | | |    ++|++   | | | | |   None   --    --
 Stationary
 
 Head           |  |  |  |    +|+++  |||||||||   Left   --    --
 Right  
 
 Left ear       |  |  |  |    +|++   | | | | |   Left  Right  Left
 Lesion
 
 Left cold      |  |  |  |    +|++   | | | | |   Left  Right  Left
 caloric
 
 Fig. 1 Discharge pattern from crista (DP), Vestibular Nuclei
 (VN),  Compensatory Eye Movement (CEM), Fast Phase Nystagmus
 (FPN)  
 
    As described above, the kinocilia of the hair cells in both
 the left and right labyrinths are on the sides of the hair cells
 toward the part of the utricle closest to the ampulla.  The
 neural activity the vestibular nuclei senses from the left and
 right horizontal semicircular canal nerves is also displayed
 (VN).  General neural activity or discharge pattern is
 represented as a train of action potentials on a single, typical
 afferent. When the head is stationary, spontaneous activity
 occurs in both the right and left vestibular nerves and the
 action potential firing frequency is equal.  This is represented
 by the two pluses, in both the right and left vestibular nuclei. 
 However, when a rightward horizontal head movement is initiated,
 the semicircular duct that is attached to the skull rotates to
 the right, but the endolymph contained within the duct, because
 of its inertial properties, tends to remain fixed in space and
 lags behind the skull movement.  In effect, this lag produces a
 relative movement between endolymph and duct wall.  This movement
 of endolymph causes the cupula partition, in the right ear, to be
 deflected toward the part of the utricle closest to the ampulla. 
 The cupula deflection causes the stereocilia to deviate towards
 the kinocilia.  
    The corresponding firing frequency in each of the nerves is
 shown in the second line of the figure.  It can be seen in this
 panel that the firing frequency decreases in the left vestibular
 nerve but increases in the right vestibular nerve.  This
 difference is indicated by an imbalance in the pluses in the left
 and right vestibular nuclei.  As the head decelerates near the
 end of the movement, the conditions reverse, and at the
 termination of the head movement, the neural activity returns to
 the spontaneous level.  In the above example, as the head begins
 to turn to the right, the eyes slowly deviate to the left in the
 horizontal plane in order to maintain stable retinal images. 
 This slow eye deviation continues until the head turn is so great
 that the eyes can no longer rotate; then they quickly return
 toward the center.  This alternation of slow deviation and fast
 return corresponds to the slow and fast phases of nystagmus seen
 during large angles of head rotation.  As the head turns to the
 right, the obvious sense of rotation of the is to the right.  
    A similar diagram could be made for pitch head movements, by
 considering the anterior semicircular canal in one and the
 contralateral coplanar posterior semicircular canal in the
 contralateral ear.
    Under certain conditions, the comparator within the central
 nervous system misinterprets the imbalance of neural activity on
 the vestibular nerves as a head turn and produces physiologically
 appropriate ocular and postural responses.  However, since the
 head is not turning, these responses are actually inappropriate
 and result in spontaneous nystagmus, perception of the visual
 surroundings as spinning, and a tendency to fall.  For example,
 in ablative lesion in the left vestibular nerve causes decreased
 neural activity in the left vestibular nerve.  An imbalance
 relative to the spontaneous discharge level in the right
 vestibular nerve occurs, and this imbalance is interpreted by the
 comparator as a head turn to the right.  Since the imbalance
 persists, the comparator interprets this as continuous head
 acceleration to the right.  Consequently, nystagmus with slow
 deviation of the eyes to the left and fast phases to the right,
 ensues.  Attempts to perform a tandem Romberg test, for example,
 would result in a tendency to fall to the left; that is, the
 postural motor response is in the same direction as the
 physiologic oculomotor response is in the same direction as the
 physiologic oculomotor response (slow phase of nystagmus).  
    The bottom line in fig 1 illustrates neural activity that
 would occur in the left and right horizontal semicircular canal
 nerves during cold, caloric irrigation of the left ear of a
 patient with normal function.  During this test, the patient
 would be lying on his or her back with the horizontal
 semicircular canals oriented vertically.  If one could view the
 horizontal semicircular canals through the top of the head and
 applied cold water to the external ear canal, the following chain
 of events could be imagined.  As the cold water cooled
 successively the lateral parts of the external canal, the
 temporal bone, and the left semicircular duct, the endolymph
 would become more dense than that contained in the utricle or the
 more medial part of the semicircular duct.  Gravity would tend to
 cause the more dense endolymph to fall and endolymph motion would
 occur in the left semicircular canal.  The cupula would thus
 deflect away from the closest part of the utricle, producing a
 decrease in the discharge firing rate in the left vestibular
 nerve relative to the spontaneous discharge in the right
 vestibular nerve and the slow phase of nystagmus (and
 correspondingly, the oppositely directed fast phase) would be the
 same as that observed during the beginning of a head turn to the
 right or during a pathologic condition resulting from an ablative
 lesion in the left vestibular nerve.  Warm irrigation of the
 external auditory meatus, through the chain of events described
 above, would cause the slug of endolymph in the lateral part of
 the semicircular canal to be less dense than that in the medial
 part.  The slug would tend to rise, and the reactions would be
 opposite to the observed for the cold caloric response. 
    The mechanisms just described provide a physiologic basis for
 responses seen in the clinic and vestibulo-ocular responses known
 to most otolaryngologists.  For example, from fig 1, one can
 predict that, generally, a peripheral ablative lesion in one ear
 will cause nystagmus to beat (fast phase will be directed) toward
 the opposite ear.  Moreover, during caloric irrigation, the fast
 phase of nystagmus will beat away from the ear irrigated by cold
 water but toward the ear irrigated by warm water.  That is, Cold
 irrigation causes nystagmus to beat toward the Opposite ear; Warm
 irrigation causes nystagmus to beat toward the Same ear (COWS). 
 Finally, during a tandem Romberg test, there is a tendency for
 the patient with an acute ablative lesion to fall toward the side
 of the affected ear.
    A similar simple diagram can be constructed for the utricle. 
 The otolith organs function is to sense the orientation of the
 head relative to gravity.  These receptors are stimulated by
 linear acceleration and tilt of the head.  Otolithic stimulation
 is thought to produce small, appropriate, compensatory eye
 movements to maintain a vertical perception of earth vertical and
 earth horizontal during pitch and roll head tilts.  There is some
 evidence that under certain situations, stimulation of the
 otolith organs can produce nystagmus.
    When the head is tipped (rolled) to the left, the otoconial
 membrane of the right utricle moves medially, while the otoconial
 membrane of the left utricle moves laterally.  The physics of
 this movement is like that of a mass on an inclined plane.  Since
 the otoconial membrane is three times the density of the
 surrounding endolymph, the force of gravity causes the otoconial
 membrane containing the tips of the stereocilia to slide relative
 to the macula in which the bodies of hair cells are embedded. 
 Thus, the stereocilia are sheared, and because of the morphologic
 and physiologic polarization discussed above, the hair cells in
 the right utricle that are on the lateral most side of the
 striola would be depolarized and those that are on the medial
 part of the utricle would be hyperpolarized.  The opposite
 conditions would occur in the left utricle.  The otoconial
 membrane movements described above would reverse for left sided
 head rolls.  Vestibulo-ocular pathways, involving the otoliths
 and the extraocular muscles, evoke counter-rotation of the eyes
 to maintain the correct visual orientation or earth vertical and
 earth horizontal.  Similarly, vestibulospinal pathways, involving
 the otolith organs and skeletal muscles, evoke postural responses
 to prohibit loss of balance.  One could draw a similar diagram to
 represent the mechanical response of the saccule during pitch
 head tilts.  During these head motions, the eyes would elevate
 and depress to maintain the earth horizon stable.  In reality,
 electrophysiologic and theoretical studies suggest that otolith,
 ocular and postural responses are not restricted to the pitch and
 roll head planes but occur in three dimensions as expected.
    During horizontal angular head movements, while the horizontal
 semicircular canals are stimulated, neither the utricle nor the
 saccule is reoriented relative to gravity.  During vertical
 angular head movements, however, both semicircular canals and
 otolith organs are stimulated since the semicircular canals are
 stimulated by the angular head motion and the otolith organs are
 reoriented relative to gravity.  Under these conditions, one
 could imagine that the otolith organs and the semicircular canals
 would work synergistically; the semicircular canals signaling the
 magnitude and direction of the angular head motion, and the
 otoliths signaling the axis about which head motion takes place.
    The mechanics of both the semicircular canals and the otolith
 organs have been mathematically modeled using a second order
 differential equation that describes the action of a physical
 system consisting of a mass, a dash pot, and a spring.  It has
 been demonstrated experimentally by recording from vestibular
 primary afferents that these models, with certain quantitative
 exceptions are generally adequate to describe the frequency
 response properties of the semicircular canals and otolith
 organs.  The predictions of these models generally support the
 idea that the semicircular canals and otolith organs operate as
 band pass filters with the "nonattenuated" part of the response
 covering the range of frequencies that comprise natural angular
 head motions and head tilts.  This range varies from one species
 to another, but in humans it ranges from 0.5 to 10 Hz.    
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                           BIBLIOGRAPHY
 
 Baloh RW, Honrubia V. Physiology of the Vestibular System. In
 Cummings CW, et al. Otolaryngology - Head and Neck Surgery:
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 Brugge JF. Neurophysiology of the Central Auditory and Vestibular
 Systems. In Paparella MM, et al. Otolaryngology: Third Edition.
 W.B. Saunders Company. 1991.
 
 Carpenter MB, Sutin J. Human Neuroanatomy. Williams and Wilkin's:
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 Correia MJ, Dickman JD. Peripheral Vestibular System. In
 Paparella MM, et al. Otolaryngology: Third Edition. W.B. Saunders
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 Lysakowski A, McCrea RA, Tomlinson RD. Anatomy of Vestibular End
 Organs and Neural Pathways. In Cummings CW, et al. Otolaryngology
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 Physiology of the Auditory and Vestibular Systems. In Ballenger
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