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J Appl Physiol 96: 2301-2316, 2004;
doi:10.1152/japplphysiol.00008.2004
8750-7587/04 $5.00
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INVITED REVIEW
HIGHLIGHTED TOPICS
Neural Control of Movement
Probing the human vestibular system with galvanic stimulation
Richard C. Fitzpatrick1 and Brian L.
Day2
1Prince of Wales Medical Research Institute, Sydney, New South Wales
2031, Australia; and 2MRC Human Movement Group, Sobell Department of
Motor Neuroscience and Movement Disorders, Institute of Neurology, University
College London, London, WC1N 3BG United Kingdom
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ABSTRACT |
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Galvanic vestibular stimulation (GVS) is a simple, safe, and specific
way to elicit vestibular reflexes. Yet, despite a long history, it
has only recently found popularity as a research tool and is rarely
used clinically. The obstacle to advancing and exploiting GVS is
that we cannot interpret the evoked responses with certainty because
we do not understand how the stimulus acts as an input to the
system. This paper examines the electrophysiology and anatomy of the
vestibular organs and the effects of GVS on human balance control
and develops a model that explains the observed balance responses. These
responses are large and highly organized over all body segments and
adapt to postural and balance requirements. To achieve this, neurons
in the vestibular nuclei receive convergent signals from all
vestibular receptors and somatosensory and cortical inputs. GVS sway
responses are affected by other sources of information about balance
but can appear as the sum of otolithic and semicircular canal
responses. Electrophysiological studies showing similar activation
of primary afferents from the otolith organs and canals and their
convergence in the vestibular nuclei support this. On the basis of
the morphology of the cristae and the alignment of the semicircular
canals in the skull, rotational vectors calculated for every mode of
GVS agree with the observed sway. However, vector summation of
signals from all utricular afferents does not explain the observed
sway. Thus we propose the hypothesis that the otolithic component of
the balance response originates from only the pars medialis of the
utricular macula.
balance; standing;
reflex; posture
GALVANIC VESTIBULAR STIMULATION (GVS) has been used for over a century as a means to
discover and then look at the function of the vestibular system. In
his 1820 dissertation, Bohemian physiologist Johann Purkyne (81)
reported that a galvanic current flowing through the head upset
balance and equilibrium. Eduard Hitzig (46),
starting his experiments as an army doctor during the
Franco-Prussian war, noted that nystagmus was one consequence of
applying an electric current to the brains of dogs and humans, including
the exposed brain of one wounded soldier. Thus we have the first
evidence that the two motor outputs of the vestibular system can be
driven by a galvanic stimulus. It was Josef Breuer (8) who
finally demonstrated the vestibular origin of these phenomena by
combining galvanic stimulation with labyrinthectomy in animals. The
first description of its perceptual output may have come much
earlier, in 1790, from Alessandro Volta himself (103). In between putting the electrodes of his newly invented battery
in his ears and his subsequent collapse, he briefly experienced the
sensations of an explosion inside his head, spinning, and the sound
of boiling tenacious matter. The spinning was likely the
manifestation of vestibular stimulation and the boiling either
auditory stimulation or the sound of flesh boiling. The explosion
needs no further explanation: a pile of 3040 Zn/Ag elements
generates 
30 V! Hitzig and Breuer also came across the perceptual
phenomenon, but they were more specific about their experiences. Camis
(10)
reported that these gentlemen put "the two electrodes to the
two mastoid processes, and experienced a sensation of falling
towards the side of the cathode."
As its early history
shows, the GVS technique is very simple. The electrodes are now
placed on the mastoid processes rather than in the ears. Just a
switch and a battery are needed, 6 V is more than enough, although
for experimental applications, the stimulus is usually delivered by
a controlled current source at levels of 1 mA. The stimulus is most commonly delivered with an anodal
electrode on the mastoid process behind one ear and a cathodal
electrode behind the other ear, i.e., bilateral bipolar GVS. However,
other configurations are bilateral monopolar GVS with electrodes of
the same polarity at both ears and a distant reference electrode and
unilateral monopolar GVS with a stimulating electrode at just one
ear. When the small current flows for 1 or 2 s, it causes a person
to sway if they are standing or perceive illusory movements if they
are not. The simplicity of the technique, however, belies the
complexity of the body response it evokes.
The virtual signal of
head movement produced by GVS has a potent effect on whole body
motor control, evoking reflex electromyographic responses and a
highly organized balance response involving the entire body. However,
these responses are not hard wired but are very sensitive to the
task at hand, the balance and orientation of the body, and the
information coming from all other sensory sources. We therefore
believe that a balance system organizes a whole body response to the
vestibular signal. It seems that the balance system interprets the
GVS-evoked input as a real head movement in space, one that was
unplanned and one that came from a movement of the body. Such an
input represents a threat to balance to which the balance system
must respond.
Apart from its
simplicity, GVS is attractive as a tool to probe vestibular function
and the balance system because it delivers a pure disturbance at the
receptor level, uncomplicated by inputs to other sensory channels. At
least in its early stages, it reveals the operation of the balance
system to a pure vestibular perturbation. The purpose of this paper
is to consider the available data on human balance responses to GVS
in light of the physiology and anatomy of the vestibular organs and
to draw some conclusions about the nature of the afferent vestibular
signal evoked by GVS and how it produces its effects on human
balance.
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VESTIBULAR ELECTROPHYSIOLOGY |
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There have been no direct recordings from human vestibular afferents; therefore,
we can only reckon their behavior by data obtained from a wide range
of species. Of extreme value here is the elegant research and
detailed electrophysiological data of Jay Goldberg and colleagues,
which include primate afferent responses to GVS.
Kinetic
Stimuli
Discharge
rates. In all species studied, the vestibular primary
afferent neurons, which innervate the cristae and maculae, discharge
spontaneously at rest when no stimulus is applied. This means that,
with rate coding, a neuron can respond to accelerations in both
directions. Spontaneous discharge rates vary across species. Mean
rates of 13 s-1 have been reported in stingrays (63),
3040 s-1 in rats and guinea pigs (14, 16),
4555 s-1 in chinchillas (38), 6590 s-1 in squirrel monkeys (28, 40),
and 90115 s-1 in macaque monkeys (15).
Regularity. Primary afferents can be classified as regular or irregular
according to the pattern of their resting discharge (28, 39, 40),
although this may be more a convenience of description, as
regularity is more a continuum than discrete populations (4, 37). The
degree of regularity or automaticity of a neuron is determined by a
combination of the size of its afterhyperpolarization relative to
the size and rate of its excitatory postsynaptic potentials (EPSPs).
Sensitivity. Afferent firing rates increase or decrease depending on amplitude and direction of an imposed acceleration. For the squirrel monkey, this dynamic range is 0300 s-1 at about the 6590 s-1 resting discharge rate, with an average gain or sensitivity of 2 s-1 per deg·s-2 for the semicircular canals and 33 s-1/g for the otolith organs (27