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line is located on or near the striola, which is a specialized section of the otolith sensory epithelium (Li, Xue,
& Peterson, 2008; Lindeman, 1969). This central region
divides the otolith into two parts, denoting the line of
polarization for each macula. The kinocilia in the utricule are oriented toward the striola, while the kinocilia
of the saccule are oriented away from the striola. As
described for the SCCs, deflection of stereocilia toward
the kinocilia depolarizes or excites the sensory cells,
while deflection away from the kinocilia hyperpolarizes or inhibits the sensory cells.
Because of the hair cell bundle orientation in the
otolith organs, every linear translation elicits both excitation and inhibition of various hair cells of the individual macula, allowing for a representation of linear
movement from each macula, as well as an integrated
representation that includes information from the contralateral otolith (Rabbitt, Damiano, & Grant, 2004).
The otolith organs are in endolymph, and the specific
gravity of the otolithic membrane is the same as that
of endolymph. Without the addition of otoconia to the
otolithic membrane, the otolith organs would not function as linear accelerometers. When a linear acceleration occurs, the otolithic membrane with its attached
otoconia lags behind that of the hair cells, transmitting
a shearing force to the underlying hair cell embedded
within the otolithic membrane (Figure 4–3) (Rabbitt
et al., 2004).
Hair Cells
Hair cells are inserted into a gelatinous structure within
each sensory end organ, the cupula in the SCCs and the
otolithic membrane in the otolith organs. There are two
types of hair cells within the vestibular system — type I
and type II (see Figure 4–1). These hair cell types differ in size and shape, as well as function. Type
cells are flask shaped and have a single, chalice-shaped
afferent nerve terminal around the base. Type II hair
cells are cylindrically shaped and have numerous bouton fibers around the base (Lysakowski, 1996; Wersäll
& Bagger-Sjöbäck, 1974). Dimorphic fibers innervate
both types of hair cells. While both type I and type II
hair cells are located throughout each vestibular sensory epithelia, the distributions vary across the region
of the sensory organ (Desai, Zeh, & Lysakowski,
2005; Fernández, Baird, & Goldberg, 1988; Fernández, Lysakowski, & Goldberg, 1995; Lindeman, 1969;
Lysakowski & Goldberg, 1997). In general, type I hair
cells are more common around the periphery. There
are approximately 23,000 hair cells located in the SCC
I hair
sensory epithelia and 52,000 located within the otolith
organs (Baloh & Honrubia, 2001).
Neural Firing
At the base of the hair cells are afferent synaptic structures that house the synaptic body, vesicles, and the
pre- and post-synaptic membranes (ribbon synapses)
(Ginzberg & Gilula, 1980; Moser, Brandt, & Lysakowski, 2006). In order for the vestibular pathway to
respond to acceleration, the cupula or otoconial membrane must be sufficiently displaced to deflect the
underlying stereocilia bundles. This mechanical action
displaces the stereocilia, and (if toward the kinocilium)
depolarizes the hair cell through a metabolic cascade
that ultimately leads to an increase in the release of the
neurotransmitter glutamate, depolarizing the afferent
nerve terminal and triggering action potentials (Barin
& Durrant, 2000).
Type I and type II hair cells provide different
information to the vestibular system due to variations
in their action potential inter-spike intervals. Type I
hair cells (with a single caliceal afferent synapse on
the hair cell) are associated with large vestibular afferents with an irregular (aperiodic) neural firing pattern, while type II hair cells (with multiple afferent
bouton synapses on the hair cell) are associated with
small vestibular afferents that display a regular (periodic) neural firing pattern (Baloh & Honrubia, 2001).
Dimorphic units (those with both caliceal and bouton
afferent endings) are of intermediate size and could be
either regular or irregular units (Baloh & Honrubia,
2001). Utilization of both regular and irregular firing
rates allows for broad representation of frequency and
acceleration information and better describes the full
range of head motion. When comparing regular versus irregular nerve fibers, there are notable functional
differences. First, irregular nerve fibers are larger and
have higher conduction velocities (Goldberg & Fernández, 1977). Irregular nerve fibers also are more efficient
at transmitting excitatory information and are more
sensitive to transient motion (Fernández & Goldberg,
1976; Goldberg, 2000).
The vestibular afferent neural system has an interesting characteristic. It has a high spontaneous resting
firing rate. This is an important feature of the vestibular system as it allows for both excitation and inhibition of each sensory end organ. The spontaneous firing
rate of vestibular neurons is between 70 and 100 spikes
per second (Goldberg & Fernández, 1971; Lysakowski,
Minor, Fernández, & Goldberg, 1995) and is somewhat
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Figure 4–3. Otolith organ anatomy and physiology. The otolith organs provide information about
linear acceleration in the horizontal and vertical planes. Hair cells within the otolith organs are oriented around the striola as demonstrated in the top left panel (in this case, with the kinocilia oriented
around the striola for utricular orientation). With the head upright and still, the hair cells remain
upright within the macula. As the head tilts forward, the otoconia pull the macula towards the ground,
thereby deflecting and depolarizing the otolith end organ.
for Medical Education and Research, all rights reserved.
higher for the SCCs (approximately 90 spikes per second) than for the otolith end organs (approximately 60
spikes per second) (Gacek, 2005; Goldberg & Fernández, 1975). Excitation of the vestibular pathway can
lead to a neural firing rate of up to 400 spikes per second (Uchino, Hirai, & Suzuki, 1982), with the contralateral inhibition reducing the discharge rate to nil.
Used with permission of Mayo Foundation
VESTIBULAR EFFERENT SYSTEM
The vestibular efferent system arises from cells on the lateral border of the abducens nucleus (CN VI) and medial
to the SVN (Carpenter & Sutin, 1983), projecting to all
five vestibular end organs. These vestibular efferents
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synapse with the calciform endings of vestibular afferents on type I and type II hair cells, as well as on type
II afferent fibers that innervate type II vestibular hair
cells (Barin, 2009; Schuknecht, 1974). Stimulation of
the vestibular efferent system in mammals results in
excitatory responses of vestibular afferents (Carpenter
& Sutin, 1983; Goldberg et al., 2012). Like the auditory
efferent system, the role of the efferent vestibular system is unknown. It has been suggested that it might
modulate the dynamic range of afferent fibers to acceleration (Carpenter & Sutin, 1983).
CENTRAL VESTIBULAR SYSTEM
As stated above, nearly all vestibular afferents synapse in the vestibular nuclei (a few project directly
to the cerebellum). From the VN, there are ascending
and descending projections that ultimately contribute to several important reflexes that are discussed in
the section “Vestibular Reflexes” (below). The central
anatomy of the vestibular system is far from simple,
and not yet completely understood. The VN receive
input from not just the vestibular nerve, but also from
the cerebellum and other sensory systems (i.e., visual
and somatosensory/proprioception). Some aspects of
vestibular stimulation are perceived, with the thalamocortical pathway subserving this perception. Additionally, there is an autonomic vestibular nervous system
which contributes to the various symptoms (including
nausea) that follow certain types of vestibular stimulation (such as that leading to motion sickness), as
well as some vascular changes in response to postural
changes. In this chapter, we can only provide a superficial review of this enormously complex system. The
interested reader can find far more detailed descriptions of the central vestibular system in the references
provided for this section.
The Vestibular Nuclei
As stated above, there are four vestibular nuclei: the
superior (SVN), inferior (IVN), medial (MVN), and lateral (LVN). As also stated above, the superior branch
of the vestibular nerve innervates the horizontal and
superior SCCs and the utricle, with a modest projection to the saccule. The inferior branch of the vestibular nerve innervates the posterior SCC as well as the
saccule. The following VN information is from Baloh
and Honrubia (2001), Carpenter and Sutin (1983), and
Kelly (1985).
The Superior Vestibular Nucleus
Much of the input to the SVN arises from the canals,
with a much more modest otolith input. There is also
substantial input from the cerebellum (from the flocculus, fastigial nucleus, nodule, and uvula). The contralateral MVN and IVN also project to the SVN.
Neurons from the SVN project to the cerebellum,
dorsal pontine reticular formation (RF), and the motor
nuclei of cranial nerves III, IV, and VI via the ipsilateral
and contralateral ascending portion of the medial longitudinal fasciculus (MLF).
The Lateral Vestibular Nuclei
The LVN (also referred to as Deiter’s nucleus) receives
primarily utricular input from the periphery and the
cerebellum (vermis and fastigial nucleus), as well as
more modest input from commissural and spinal fibers.
The output of the LVN is largely the ipsilateral
vestibulospinal tract (VST) (ending in the spinal cord
at the cervical, thoracic, and lumbar levels), as well as
some efferent projections via the MLF bilaterally to the
oculomotor nuclei.
The Medial Vestibular Nuclei
The MVN receive small diameter vestibular nerve fiber
afferents from the SCCs as well as the otolith organs.
Other inputs to the MVN include the contralateral
MVN, the RF, and the cerebellum (fastigial nucleus,
flocculus, nodule). Outputs from the MVN include
efferents that travel in the MLF as the medial VST to
cervical (and by some accounts thoracic) levels of the
spinal cord. Other efferents include those to the oculomotor nuclei via the ascending MLF, as well as to the
contralateral VN, the RF, and the cerebellum.
The Inferior Vestibular Nucleus
The inferior (or descending) VN inputs are from the
ipsilateral canals and both otolith organs, the contralateral VN (all four major nuclei), as well as from the
cerebellum (uvula, nodule, flocculus). In ventrolateral
and caudal IVN, there is a group of cells (group f) that
arise from the cerebellum and receive no input from
vestibular afferents.
The efferent fibers from the IVN project to the contralateral VN, the cerebellum, and the RF.
The Interstitial Nucleus of the Vestibular Nerve
There are other groups of cells associated with the
VN. We will limit our discussion here to the intersti-
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tial nucleus of the vestibular nerve (INVN). The INVN
is a group of cells in the vestibular nerve near where
the nerve enters the brainstem. In chinchilla, it receives
mostly otolith input, and efferent fibers from the INVN
enter the ascending MLF.
The Cerebellum
There is a rich bidirectional connection between the
VN and the cerebellum. Primary vestibular afferents
pass through the SVN and LVN and enter the cerebellum, and primarily project to the ipsilateral cerebellar
cortex (flocculus, nodulus, uvula; Carpenter & Sutin,
1983; Watson, 1991). The saccule and utricle provide
the predominant vestibular input to the cerebellum
(Pansky, Allen, & Budd, 1988). As described by Fetter and Dichgans (1996), the vestibulo-cerebellum has
reciprocal connections between the cerebellum (vermis
and flocculus) and the vestibular organs, the VN and
pontine RF. The cerebellar flocculonodular lobe projects to neurons whose axons are from the reticulospinal
tract (RST) and the lateral vestibulospinal tract (LVST).
Fibers from the cerebellar fastigial nucleus project to the
VN as well as the RF (the lateral reticular nucleus and
nucleus reticularis pontis caudalis; Pansky et al., 1988).
The Reticular Formation
The cells of origin of the RST arise from the bulbar
(pontomedullary) RF (Fetter & Dichgans, 1996). The
input to the pontomedullary RF neurons is predominantly from the otoliths, but RF input arises from all
four VN. RST fibers are both crossed and uncrossed,
and extend the length of the spinal cord (Fetter & Dichgans, 1996; Honrubia & Hoffman, 1997). Goldberg et
al. (2012) have identified two RSTs: the medial (MRST)
and lateral (LRST) tracts. MRST fibers arise from the
nucleus reticularis pontis caudalis, nucleus reticularis
pontis oralis, and rostral portions of the medullary
nucleus reticularis gigantocellularis, and enter the ventromedial funiculus of the cervical spinal cord. LRST
fibers arise from more caudal portions of the medullary
nucleus reticularis gigantocellularis and nucleus reticularis ventralis, and enter the ventrolateral funiculus of
the cervical spinal cord. Some VST fibers terminate at
cervical or thoracic levels, while others continue to the
lumbar spinal cord (Goldberg et al., 2012). Projections
from the vestibular pathway to the bulbar RF lead to
sweating and nausea/vomiting during vestibular stimulation (such as occurs with motion sickness) (Pansky
et al., 1988).
Thalamocortical Projections
There are challenges when studying the thalamocortical vestibular system. This is in large part due to the
great diversity across mammalian neocortex, which
is no doubt complicated by the fact that human are
bipeds, and all mammalian animal models used to
study the vestibular system are quadrupeds.
The VN have thalamic projections that include the
ventroposterior nucleus, with extensions into the ventrolateral nucleus and posterior thalamic group. These
thalamic regions project cortically into the parietoinsular vestibular cortex (PIVC) postcentral area 2v and
postcentral area 3a (known as area 3av). The thalamic
ventrolateral nucleus also projects to premotor and
motor cortex and receives input from deep cerebellar
nuclei (Goldberg et al., 2012).
As summarized by Baloh and Honrubia (2001),
the vestibulothalamocortical pathway includes (in
non-humans):
i. The VN (from the LVN and SVN)
ii. The thalamic ventralis posterior lateral pars oralis
nucleus (as well as a smaller projection that runs
with the auditory projection to the medial geniculate body)
iii. Cortical projections, including (a) near the central
sulcus close to the motor cortex, and (b) the inferior
intraparietal sulcus close to face area of the postcentral gyrus of the primary sensory cortex
As also summarized by Baloh and Honrubia
(2001), galvanic stimulation of the superior Sylvian
gyrus and inferior intraparietal sulcus produces the
sensation of rotation or body displacement. Bilateral
galvanic stimulation of the vestibular system revealed
functional magnetic resonance imaging activation of
the posterior insula (PIVC), Heschel’s gyrus (transverse temporal), and the pulvinar of the thalamus. In
animal studies, Baloh and Honrubia (2001) reported
that thalamic and cortical units that respond to vestibular stimulation also commonly respond to visual and
proprioceptive stimuli.
The thalamocortical projections travel throughout
the cortex, including the hippocampus. The hippocampus is associated with spatial perception and cognition,
particularly as it relates to spatial orientation. Damage
within the vestibular system and along this pathway
has been associated with deficits in spatial memory
(e.g., Bigelow, Semenov, du Lac, Hoffman, & Agrawal,
2016; Brandt et al., 2005; Semenov, Bigelow, Xue, du
Lac, & Agrawal, 2016). Aitken, Zheng, and Smith (2018)
provide a review of the influence of vestibular system
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input on hippocampal function as well as functional
outcomes of deficits along this pathway.
Berthoz (1996) summarized the results of several
studies that demonstrated descending projections from
cortex to the brainstem (and VN). One of these studies
(Faugier-Grimaud & Ventre, 1989) found direct projections from posterior parietal area 7 to more caudal
areas, including the VN (including the IVN, MVN and
SVN) in Macaca fascicularis (the crab-eating macaque).
The Autonomic System
Goldberg et al. (2012) describe three pathways involved in
what they term the “vestibulo-autonomic connections”:
i. A VN to nucleus of the solitary tract that projects
to nuclei in the brainstem involved in autonomic
function, including ventrolateral medulla and the
dorsal motor nucleus of the vagus nerve.
ii. A pathway from the VN to the pontine parabra-
chial complex. Additional inputs to the parabrachial complex include visceral and gustatory
information from the solitary nucleus.
iii. The cerebellar cortex is thought to contribute to the
brainstem autonomic circuits, as respiratory and
cardiovascular effects have been related to cerebellar function.
Afferent and efferent vagus nerve activation can lead
to symptoms that occur prior to vomiting (e.g., sweating, salivation, increased blood pressure, heart rate
changes, decreased gastrointestinal motility) that are
known to be mediated by the autonomic nervous system (Babic & Browning, 2014; Singh, Yoon, & Kuo,
2016). Yates, Bolton, and Macefield (2014) have provided a detailed review of the vestibulo-sympathetic
responses. They reviewed the literature that convincingly demonstrates that the vestibular system (specifically the otolith organs) contributes to the sympathetic
control of blood pressure during movement and postural changes. They also highlight some differences in
vestibulo-sympathetic responses in humans and experimental animals, and noted that cognitive factors can
modulate the gain of vestibular-sympathetic responses.
VESTIBULAR REFLEXES
Let us briefly move away from talking about the vestibular system to the topic of gait. Walking in bipeds
can be viewed as controlled falling. While standing
upright, our center of pressure is over our base of support (see Chapter 5 for more details). When we take a
step, we must move our center of pressure outside our
base of support, quickly adjust our center of pressure
over the new base of support, and continue this process
as we move forward. We also need to monitor where
we are in space, and so our three main sensory systems used for balance are actively part of the complex
motor plan that keeps our controlled fall from becoming an uncontrolled fall. The sensory systems include
vestibular (of course!), vision, and proprioception
(again, see Chapter 5 for more details). As we walk,
our proprioceptive system tells us about the orientation of our body in space. The orientation of the head
relative to the body is provided by neck proprioception, our vestibular system (mainly the otolith organs)
tells us whether we are aligned with the gravity vector,
while vision tells us how our head is oriented relative
to the visual target (perhaps the end of the road we are
walking on). Our head is moving up and down, left to
right, as we move forward, requiring small but important adjustments of our head and eyes to keep our gaze
centered on our selected visual target. We also make
decisions as we walk, changing what we are looking
at (perhaps we hear a sound to our left and want to
see what that is, and make the conscious decision to
move our gaze to the left). We might keep our head
fixed and move our eyes to the left, or we might move
our head to the left and keep our eyes fixed ahead.
These latter activities involve conscious decision making that no doubt involves the thalamocortical system
discussed above. Thus, the conscious decisions made
while walking (and during other motoric activities)
must have some control over the stereotypic reflexive
activity that keeps our base of support over our center
of pressure and our gaze fixed on the desired target. As
you can see, walking is a very complex motoric activity, which is highly multisensory and involves sensorymotor integration (and thus the cerebellar involvement
as discussed above), as well as coordination of reflexive
activities with conscious decision making.
We will (below) discuss several basic reflexes that
involve the vestibular system. These are often simplifications of a more complex process. For example, for the
vestibulo-ocular reflex (VOR), we limit our discussion
to angular head movements in the horizontal plane,
rather than include movements in the other planes.
This is for the sake of simplification, as movements in
the vertical plane will involve other end organs, perhaps other vestibular nuclei, and certainly other oculomotor nuclei and extraocular muscles. We are also not
including all possible contributors to these reflexes. For
example, we know there are projections to and from
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the cerebellum to the vestibular system, and that the
thalamocortical system has connections with the vestibular system (see central anatomy sections above),
but they will be ignored in our simplified descriptions
below. Finally, we have gaps in our knowledge about
these complex reflexes. This is especially true for the
descending reflexes, such as the vestibulospinal reflex
(VSR). While the general pathways are known, details
about these reflexes in animal models using invasive
studies not possible in humans are not always easily generalizable from animals to humans. This is
because humans are the only true mammalian bipeds,
while most animal models (other mammals, including
rodents) are quadrupeds, and even monkeys are typically quadrupeds that at times become bipeds. While
sophisticated non-invasive techniques are available to
study human vestibular reflexes (e.g., motion analysis,
electromyography, functional imaging), there are often
gaps in this human-based knowledge.
The Vestibulo-Ocular Reflex
A schematization of the VOR is shown in Figure 4–4.
The following description of the VOR is adapted from
Furman and Cass (2003). When we move our head to
the left, for example, the response to this counterclockwise rotation is to increase the discharge rate of the left
horizontal SCC and decrease the discharge rate of the
right horizontal SCC. As noted above, this push-pull
discharge rate of complementary canals is a fundamental property of the vestibular system. In Figure 4–4 , the
upward and downward arrows reflect increased and
decreased neural discharge, respectively. The superior
vestibular nerves (bilaterally) project to the VN and
then cross via the MLF to innervate the contralateral
abducens (CN VI) nuclei. CN VI nuclei project to the
lateral rectus (LR) on the same side (ipsilateral to CN
VI, but contralateral to the horizontal canal providing the neural input). Also, from each CN VI, there is
a contralateral projection to the oculomotor (CN III)
nuclei, which each project to the ipsilateral (now relative to both the oculomotor nucleus and the driving
horizontal canal) medial rectus (MR) muscle of both
eyes. Now let us follow what is happening in this figure. The increase (or decrease) in superior vestibular
nerve discharge rate is reflected in VN, CN VI, and
LR activity (i.e., the contralateral projections), while
this sign (increased versus decreased) of peripheral
nerve activity is reversed with the double crossing
Figure 4–4. The vestibulo-ocular reflex (VOR) pathway. Abbreviations: VN: vestibular nuclei; CN VI: cranial nerve
VI; CN III: cranial nerve III; MLF: medial longitudinal fasciculus; LR: lateral rectus muscle; MR: medial rectus muscle.
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(and hence ipsilateral projections) that ultimately end
in the MR muscles. Note that absolutely no inhibitory
interneurons are shown in this schematic, meaning that
this entire reflex can be explained by maintaining the
increase or decrease in discharge rate by both crossed
and uncrossed fibers.
Ultimately, the head turn toward the left leads
to the eyes turning to the right, the result of the left
MR and right LR contracting, and the left LR and right
MR relaxing. This achieves the very laudable goal of
this reflex: to a head turn, the eyes should move in the
opposite direction (and hopefully of equal magnitude)
that will keep the fovea of the retinas on the visual target of interest.
The Vestibulocollic Reflex
The vestibulocollic reflex (VCR) stabilizes the head
by activation of the neck muscles (Hain & Helminski,
2014). Hain and Helminski (2014) have noted that the
reflex pathway is not known in detail, while Schubert
and Shepard (2016) indicate that this reflex is mediated
through the otolith organs and the MST. It seems clear
then that we can use the available data on the pathways
of the cervical vestibular evoked myogenic potential
(cVEMP) as one possible (but likely) pathway for the
VCR, as the cVEMP arises from the otolith organs and
can be recorded as a muscle response in two major
muscles of the neck: the trapezius and the sternocleidomastoid. For more information about the cVEMP, see
Chapter 16. The proposed pathway of the VCR would
be the otoliths (likely primarily the saccule), the inferior
(and perhaps some input from the superior) vestibular
nerve(s) to the MVN, to the accessory spinal nucleus of
CN XI, and to the trapezius and sternocleidomastoid
muscles. This is just one of several possible pathways,
as other muscles may be involved in the stabilization
of the head and neck. There is likely additional input
from the canals so that head movement can reflect both
linear and angular acceleration, and there are two other
pathways with vestibular inputs descending through
the neck region other than the MVST (i.e., the LVST
and the RST). Goldberg and Cullen (2011) provide a
detailed presentation on the VCR.
The Vestibulospinal Reflex
Acceleration of the head often causes upper and lower
limb responses, with the limbs in the direction of the
acceleration extended, while those contralateral to the
direction of movement contracted (Schubert & Shepard,
2016). The VSR maintains the center of pressure over the
base of support (see Chapter 5) and thus, in more practical terms, prevents us from falling. With this in mind,
there is likely a family of VSRs used depending on the
nature of the perturbation as well as the strategy chosen
to maintain balance. Desmond (2004) noted that there
are several strategies to maintain balance post-perturbation, including: (1) the ankle strategy of the lower leg
muscles if the perturbation is not too large; (2) the hip
strategy involving the hips and upper body for larger
amplitude displacements; (3) a suspensory strategy
that involves lowering the center of gravity (e.g., squatting); and (4) the stepping strategy, i.e., taking a step in
the direction of the perturbation and thus putting one’s
center of pressure back within the base of support.
Hain and Helminski (2014) noted a number of
factors that would likely change the specific vestibulospinal reflex (VSR) pathway (including whether the
sensory input is canal and/or otolith), and provided
an example of one VSR. In this example, in response to
a lateral head tilt (with both canal and otolith stimulation), the resulting end organ activity projects to the VN
(and specifically to both the LVN and MVN), projecting
to the spinal cord via the LVST and MVST to muscles
of the trunk and/or lower limbs. Muscles on the side of
the direction of head tilt would go into extension, while
muscles on the opposite side would flex. The specific
muscles activated would of course depend on the magnitude of the perturbation and the strategy used to prevent a fall. If that strategy were limited to lower limb
activity, it would likely not involve the MVST, as that
only projects as far as the cervical spinal cord, or the
thoracic cord (depending on whose article or chapter
you choose to believe).
PRACTICAL IMPLICATIONS FOR
VESTIBULAR
The vestibular system encodes head and body acceleration cues and sends this information into the central nervous system. When this system is functioning
appropriately, vestibular system information integrates
with other sensory systems, such as the visual and proprioceptive systems, in order to maintain balance and
stabilize gaze. While we often focus on the clinical evaluations of these underlying vestibular end organs and
reflex pathways, we must also consider what happens
to this information once it is integrated by the central
nervous system. Emerging research is expanding our
understanding of how vestibular system information
contributes to multisensory integration and orientation, as well as cognitive function.
SYSTEM FUNCTION
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Spatial Orientation
We use vestibular system information in order to
maintain a sense of spatial orientation — the ability to
maintain body orientation relative to the surrounding
environment. The vestibular system provides the information required to model the environment. This information is transmitted through the vestibular nerve
to the brainstem and cerebellum and subsequently
through the hippocampus (Maguire, Frackowiak, &
Frith, 1997) or thalamus to the parietal insular vestibular cortex (Dieterich & Brandt, 2018). Atypical function
anywhere along these pathways may lead to a sense
of dizziness or spatial disorientation (Cronin, Arshad,
& Seemungal, 2017), leaving an individual unable to
determine his or her body position or motion relative
to the environment.
While patients with vestibular dysfunction may
report a sense of disorientation, especially when in
vision-denied conditions (Whitney, Sparto, Cook, Redfern, & Furman, 2013), spatial disorientation can happen even to those with typically functioning peripheral
and central vestibular systems. Aviators find this especially problematic, as visual and vestibular inputs are
often incongruent, posing a significant safety issue.
Thirty percent of all fatal aviation accidents are associated with spatial disorientation (Gibb, Ercoline, &
Scharff, 2011). In order to address the risk of spatial
disorientation, pilots are exposed to training paradigms that focus on using the cockpit instruments and
overriding visual or vestibular sensory information
(Haslbeck & Zhang, 2017; Ledegang & Groen, 2018).
Discounting internal (vestibular) and external (visual)
cues in place of technology is quite challenging, and
spatial disorientation continues to be a significant concern for aviators. Research continues into understanding how vestibular sensory information may reduce
this significant safety issue.
Multisensory Integration
Maintaining spatial orientation requires the integration
of various sensory systems, including the vestibular,
visual, and proprioceptive systems. The vestibular system is a silent contributor to this multisensory integrator, as we only are aware of it when it malfunctions and
provides inaccurate information. The resulting sense
of dizziness or imbalance is commonly the reason for
a patient to present to the vestibular clinic; however,
there are various situations where we may become
acutely aware of this multisensory integration in
everyday life activities. The most common abnormal-
ity associated with multisensory integration is motion
sickness. Motion sickness occurs due to multisensory
conflict, meaning that information from the vestibular,
visual, and proprioceptive systems is not in agreement
(Reason & Brand, 1975). Atypical processing of sensory
information within the velocity-storage mechanism
and cerebellum has been associated with motion sickness. When incongruent visual and vestibular information is identified in the cortex, autonomic and nausea
processing centers are triggered (Toschi et al., 2017),
leading to symptoms such as sweating, headache, nausea, and vomiting. For a review of the underlying neural basis of motion sickness, see Cohen and colleagues’
recent work (Cohen, Dai, Yakushin, & Cho, 2019).
Motion sickness is common in the general population and approximately 13% of individuals report some
level of motion difficulty (Huppert, Grill, & Brandt,
2013). Patients presenting to the vestibular clinic may
be more likely to present with history of motion sickness (31%). Furthermore, self-reported motion sickness
may be highest in patients diagnosed with vestibular
migraine (56.9%) and benign paroxysmal positional
vertigo (48%), as well as in approximately one-third of
patients diagnosed with orthostatic dizziness, Ménière’s
disease, functional dizziness, and unilateral vestibulopathy (Strupp, Brandt, Huppert, & Grill, 2018). This
increased presentation of motion sensitivity for patients
in the vestibular clinic is reasonable to expect, as atypical sensory integration may be due to abnormal or
inconsistent peripheral vestibular dysfunction or aberrant central integration mechanisms (Strupp et al., 2018;
Wang & Lewis, 2016).
Motion sickness can be triggered by various stimuli associated with transportation, such as cars, trains,
planes, and boats. As humans moved to the more challenging environment associated with space exploration, the importance of gravity
discovered to influence motion sensitivity in microgravity environments (Bles, 1998). After entering
microgravity, the otolith organs are “off-loaded,”
meaning that they no longer are sensitive to gravity
as they are on earth. Astronauts report a sense of spatial disorientation at this transition and some describe
a sense of tumbling backward as well as a sensation of
being upside down (Young, 2000). Over the first few
hours to days, approximately 70% of those entering
microgravity experience symptoms of “space” motion
sickness (Lackner & Dizio, 2006), with comparable gastrointestinal symptoms such as nausea and vomiting
as motion sickness experienced on earth (Thornton &
Bonato, 2013). Motion sickness can impede important
work timelines during short missions (Jennings, 1998;
Thornton & Bonato, 2013). Microgravity is an extreme
— or lack thereof — was
82 BAlAnCE FunCtion AssEssmEnt And mAnAgEmEnt
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environment that few will experience. Nonetheless,
understanding how the vestibular system adapts to
microgravity is essential in advancing our understanding of these complex systems.
With advances in technology, more of the general
population will be exposed to situations that may lead
to motion sickness. Video games, three-dimensional
movies, and virtual reality provide new opportunities
for sensory conflict as the movement of the visual field
is misaligned with information provided by the vestibular and proprioceptive systems (Munafo, Diedrick,
& Soffregen, 2017). Individuals watching three-dimensional movies have demonstrated significantly more
symptoms consistent with motion sickness as well as
symptom severity that is nearly nine times higher than
baseline compared with watching a two-dimensional
movie (Solimini, 2013). Women and those with known
motion sensitivity may demonstrate a higher risk for
motion sickness in virtual reality environments (Munafo
et al., 2017; Solimini, 2013). Research to mitigate these
effects continues, with reduced motion sickness symptoms reported in cases where the vestibular and visual
systems are “recoupled” using techniques such as galvanic vestibular stimulation (Cevette et al., 2012, 2014)
or additional movement aligned with the visual field
(Aldaba, White, Byagowi, & Moussavi, 2017).
Cognitive Impact
One might not expect the vestibular system to influence cognitive function, but the vestibular system is
intricately involved in providing information throughout the cortex. There are several concepts to consider
when evaluating vestibular system input on cognitive
function. Foremost is the concept of balance and cognitive load. This “posture-first” principle states that
maintaining appropriate stance or balance is of primary
concern and that neurological processing resources
may be recruited to maintain balance regardless of any
additional cognitive load (Lajoie, Teasdale, Bard, &
Fleury, 1993). For example, an individual may be able
to walk briskly down a hallway and calculate mathematical problems easily; however, that same individual
will likely have considerable difficulty completing the
same mathematical task while walking across a frozen
sidewalk. The act of walking when the ground is slippery now requires additional cognitive resources, pulling from those previously available and allowing the
individual to remain upright. As cognitive resources
are limited, in this example the additional cognitive
resources required to maintain balance on the frozen
sidewalk leave minimal resources for performing the
mathematical calculations. This is known as the dual
task paradigm. Limited cognitive resources become
especially important when considering the impact of
aging on reduced vestibular function and diminished
cognitive resources (Semenov et al., 2016), as well as
for patients with reduced cognitive capacity, such as in
Alzheimer’s disease. These patients may have impaired
balance due to the limited cognitive resources available
to shift over toward balance maintenance under typical
or challenging conditions (Barra, Bray, Sahni, Golding,
& Gresty, 2006).
There are other considerations related to cognitive performance to consider in the vestibular clinic
and laboratory. Ongoing research is providing a clearer
understanding of how vestibular information influences cognition (Bigelow et al., 2016). The vestibular
system may be specifically involved in cognitive function as it relates to spatial memory (Smith, Wilkinson,
Bodani, Bicknell, & Surenthiran, 2018). Additionally,
individuals with vestibular dysfunction describe having difficulties in concentration and memory, as well as
limitations in activities of daily living due to memory
concerns or confusion (Bigelow et al., 2016). Those with
vestibular impairments reported reduced activities of
daily living associated with cognitive tasks and not
necessarily those based on movement (Harun, Oh, Bigelow, & Agrawal, 2017). Furthermore, individuals with
vestibular dysfunction may also demonstrate greater cognitive impairment than expected for their age (Semenov
et al., 2016). The cognitive impairment associated with
vestibular dysfunction has generally been associated
with altered neural modulations or significant changes
in cortical structures such as the hippocampus and
thalamus in those with peripheral vestibular dysfunction (Aitken et al., 2018; Brandt et al., 2005; Hüfner et al.,
2007). Reviews of this emerging area have been provided by Bigelow and Agrawal (2015) and Smith (2017).
Individuals with vestibular dysfunction are more
likely to demonstrate reduced ability to complete
activities of daily living and are at higher risk of falls.
Therefore, patients with both dizziness symptoms and
cognitive concerns are likely to present to the vestibular
clinic. The addition of questionnaires, such as the Montreal Cognitive Assessment (MoCA) (Leandri, Campbell, Molfetta, Barbera, & Tabaton, 2015) and Saint
Louis University Mental Status examination (SLUMS)
(Cummings-Vaughn et al., 2014), would be a reasonable addition for vestibular clinics evaluating adults
at risk for cognitive impairment. These questionnaires
can provide the clinician with important information
about the patient and may alter referral recommendations for cognitive concerns or rehabilitation options.
Clinical testing in patients with cognitive impairment
4. PrACtiCAl AnAtomy And PHysiology oF tHE vEstiBulAr systEm 83
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may be hindered due to patient limitations. For example, some patients with significant cognitive impairment may not be able to complete the required tasks for
vestibular testing, especially when required to maintain a specific eye or body position (Harun et al., 2017).
Further research in the area of cognitive function and
the vestibular system will no doubt provide substantial changes to our understanding of central vestibular
pathways and pathology.
summary
The vestibular system is uniquely designed to detect
head accelerations across the broad range of typical
human activities. The vestibular end organs provide
key sensory information about both angular and linear
accelerations. This information is encoded to appropriately keep our center of pressure over our base of
support (i.e., keep us from falling) as well as maintain
appropriate gaze stability during motion. Understanding the underlying anatomy and physiology of this
complex sensory system allows for the clinician to better understand how to evaluate and manage disorders
associated with the vestibular system.
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