Miles & Lisberger, ARN

Ann. Rev. Neursci 1981.
4:273-99
PLASTICITY IN THE
VESTIBULO-OCULAR REFLEX:
A NEW HYPOTHESIS
+
F A. Miles and S G. Lisberger
Laboratory of Neurophysiology, National Institute of Mental Health,
Bethesda, Maryland 20205
INTRODUCTION
+11555
Eye movement recordings reveal that we do not scan our visual surround
ings like the cinecamera panning across a scene, but rather take in the view
in a sequence of still-shots. Visual search is a speculative business and
several times a second throughout the waking hours we generate rapid
saccadic eye movements that relocate the image of the world on the retina.
In this way, images that may prove to be of particular interest are positioned
in the fovea-the region of most acute vision-for detailed scrutiny. If this
detailed processing of the retinal images is to proceed efectively, then the
eyes must be stabilized with respect to the surroundings. Indeed, visual
acuity begins to deteriorate appreciably when the retinal images drift at
more than a few degrees per second (estheimer & McKee 1975). Head
movements pose a serious potential threat to ocular stability and are dealt
with by a refex that generates compensatory eye movements to ofset them:
the vestibulo-ocular reflex (VOR).
A striking feature of the VOR is that it operates without the beneft of
immediate feedback. The input to the system, head rotation, is sensed by
the semicircular canals, whose primary aferent discharges supply the brain
stem with frequency-coded information efectively describing the head's
angular velocity. A variety of direct and indirect neural pathways then
convey these signals to the motoneurons innervating the extental eye mus
cles that generate the ouput, compensatory eye rotation (see Figure 1).
Because the output of the refex does not infuence the receptors sensing the
input, the VOR is said to operate as an open-loop control system. A major
problem shared by all such systems is calibration: How is the performance
+
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copyright covering this paper.
273
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Quick links to online content
Further
ANNUAL
REVIEWS
274 MILES & LISBERGER
regulated so that the counter-rotations of the eyes do indeed accurately
compensate for the rotations of the head? Although this problem had been
clearly enunciated by R0nne i 1923, it was not generally recognized until
very recently. The prevailing assumption-implicit i not explicit-was that
the refex was "hard-wired" and presumably genetically specifed; the prob
lem of establishing and maintaining appropriate performance levels was not
generally appreciated. Gonshor & Melvill Jones (1971) fi rst demonstrated
the fallacy of this notion about a decade ago, when they found that the VOR
underwent extensive changes when subjects wore left-right, reversing-prism
spectacles and even showed reversal under some circumstances (Gonshor
& Melvill Jones 1976b). This led to the suggestion that the VOR was subject
to long-term regulation by some visually mediated adaptive process whose
normal function was to keep the system appropriately calibrated. The seem
ingly machine-like quality of the VOR engendered the hope that it might
eventually prove to be a model system for studying cellular mechanisms
underlying memory and learing in the central nervous system.
A adaptive capability has now been demonstrated in the VOR using a
range of optical techniques in a variety of animals. However, some species
diferences concering the detailed mechanisms are beginning to emerge,
and in order to avoid confusion we have structured our review around the
A.
Head Rotation
B.
in World

Eye Rotation
in Head
r---------------------
I I
I Ihw
I
I
h
w
l 8h 1+ e
w
. L. -j----
Semicircular Brain Orbit
Canal
Figure 1 The VOR a an open-loop control system. A: Basic neuronal organization (much
simplifed). B: Block diagram; continuous lines denote signal fow channels within the nervous
system; dicontinuous lines repreent exteral, physical links denoting head velocity with
repet to the world (hw). eye velocity with respet to the head (eh) and eye velocity with
respect to the world (cw gaze velocity).
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PLASTICITY IN VESTIBULO-OCULAR REFLEX 275
work on the monkey; in general, only passing reference is made to the work
on other animals. As yet, no biophysical or morphological correlates of
these adaptive changes have been found in any species and the major
concers remain the general nature of the adaptive mechanism and the site
of the modifiable elements. At least insofar as the monkey is concered,
many of the initial ideas about the adaptive mechanism. particularly the role
of the cerebllum, do not apply, and we shall propose a new hypothesis.
GENERAL NATURE OF THE VOR
Short-Term Operation
Before proceeding to consider the long-term regulation of the VOR, it is
imperative to understand the general workings of the normal refex. Insofar
as the structural organization of the system is concered, we need consider
only the rudiments. Extensive treatments of the neural circuitry and signal
processing are available in several excellent reviews (Carpenter 1977, Cohen
1974, Precht 1979, Wilson & Melvill Jones 1979).
MACHINE-LIKE OPERATION Three notable features of the primate
VOR that together give it a machine-like appearance are its high speed,
accuracy, and consistency. The combination of a virtually instantaneous
inertial receptor organ, shor central pathways with few synaptic delays,
and an extremely rapid plant (the extraocular muscles and eyeball) pro
duces a total delay of only 1 2 msec from head movement to compensatory
eye movement (F. A. Miles and S. G. Lisberger, in preparation). (Note that
a car travelling at 55 mph would manage to travel only 1 f in that time!)
It is usual to assess the performance of the refex by recording the compen
satory eye movements resulting from passive sinusoidal oscillation of the
whole animal about the vertical axis in the dark. Over the frequency range
of 0.1 to 1 .0Hz, the gain of the rhesus monkey's VOR, defned as peak eye
velocity divided by peak head velocity, is usually 0.9 to 1 .0; with standard
deviations typically less than 5% of the response, the system can be said
to deserve the description "machine-like" (Miles & Eighmy 1980). In the
rhesus monkey, therefore, preservation of a stable retinal image during head
turs can be accounted for almost entirely by the operation of the VOR.
Other mechanisms-proprioception, preprogramming, and vision-are
very minor (Bizzi et al 1972).
VISUAL FEEDBACK: A POOR SUBSTITUTE FOR THE VOR In the light,
visual feedback mechanisms in the form of the pursuit and optokinetic
systems are also available to stabilize the eyes with respect to the surround
ings. Operating in the manner of negative-feedback tracking systems, they
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respond to the slippage of retinal images by generating eye movements that
tend to reduce that slip. All animals with mobile eyes appear to have an
optokinetic system that responds to wide-field image motion across the
whole retina. Since it is responsive to movements of the background images
such as those that would occur if the VOR failed to completely stabilize the
eyes during head turs, the optokinetic system operates to reduce any
residual retinal image slip and therefore can be regarded as a back-up to the
VOR; however, the optokinetic system is so slow that it remains a poor
substitute for a appropriate VOR. The same is true, though perhaps to a
lesser extent, of the pursuit system, which so far has only been found in
higher vertebrates. This system is especially responsive to small moving
images in the foveal region and allows the animal to track small objects even
when they cross a featured background. Success here means overriding any
optokinetic "resistance" that the movement of the eyes relative to the
stationary background would normally elicit. However, for the present this
is of less concer to us than the fact that, when not being used to track
moving objects, the pursuit system will be available to act in concert with
the optokinetic system to aid stabilization of the eyes with respect to the
surroundings. Even when the two systems operate together in this fashion,
minimal latencies from slip to onset of tracking eye movement are still in
excess of 80 msec (Lanman et al 1978). Thus, extensive dependence upon
visual feedback would clearly mean that the animal would have to endure
considerable motion of its visual world during fast head turs, which would
severely compromise its visual acuity. These limitations of the visual feed
back mechanisms obviously make it all the more imperative that the VOR
should be appropriately calibrated.
An obvious additional advantage of a nonvisual mechanism such as the
VOR for maintaining ocular stability is that it continues to function in
low-luminance conditions. Furthermore, the VOR has great utility in situa
tions where the light levels are adequate but the environment lacks the
textural features needed for visual stabilization, e.g. the open-water habitat
of the pelagic fish. These situations emphasize the feedforward nature of the
refex since its purpose here is obviously not to stabilize nonexistent or
featureless images but rather to insure that, if something should come into
view. its image will fall upon a reasonably stable retina.
VOR FNCTIONS TO STABILIZE RETINAL IMAGES BY PRESERVING
GAZE VELOCITY Ordinarily, when we refer to "eye position," we mean
"position of the eyes with respect to the head." However, in discussing
eye-head coordination it is also important to consider "position of the eyes
with respect to the surrounding world," to which we refer as "gaze posi
tion." For various reasons that will gradually become apparent, the VOR
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is most readily dealt with in the velocity domain so that we shall mostly be
referring to eye velocity, gaze velocity, etc. Algebra defnes gaze velocity
(abbreviated to ew, to denote eye velocity with respect to the world) as the
sum of (a) the velocity of the eyes with respect to the head (eye velocity,
h) and (b) the velocity of the head with respect to the world (head velocity,
hw)
:
Gaze velocity (ew) eh + hw. 1.
The function of the VOR in simple situations where the animal is viewing
the stationary surroundings can now be restated: to keep gaze velocity
(ew) zero by insuring that any changes in head velocity (hw) are always
ofset by converse changes in eye velocity (eh)' The ultimate aim, of course,
is to prevent movements of the head from disturbing the stability of the
retinal image of the surroundings. However, the VOR continues to be
equally important when the monkey uses its pursuit system to track small
moving objects, a situation in which the monkey is now more interested in
stabilizing the image of the moving target than the image of the stationary
surroundings. The animal's performance in such situations is measured by
how well it manages to match its gaze velocity (eye velocity with respect
to the world) to the target's velocity (measured with respect to the world),
and this is known to be protected by the VOR against any disturbance
resulting from movements of the head (Lanman et al 1978). Two systems
sharing the common fnal pathway are at work here (see Figure 2): (a) the
negative-feedback pursuit system, which attempts to match gaze velocity
(ew) to target velocity (lw), and (b) the open-loop VOR, which operates to
protect the gaze velocity !ew) generated by the pursuit system against
changes in head velocity (
h
w)' The extraordinarily brief delay in the ves
tibulo-ocular response (about 12 msec) ensures that any disturbance of the
head will cause only brief interruptions-largely trivial-in the animal's
pursuit of the target.
Of course, the monkey may choose to pursue moving targets by combin
ing smooth movements of both its eyes and head (Lanman et al 1978),
although the latter will be ofset by the compensatory eye movements
generated by the VOR. Indeed, the VOR might seem to be counter-produc
tive here, since in efect it cancels any contribution that the head movement
might otherwise have made to the pursuit. Thus, at first glance, one might
think that it would be in the system's interest to reduce the gain of the VOR
in these circumstances. However, any such change would mean that unfor
seen disturbances of the head would be inadaequately compensated and so
would severely compromise tracking performance. This is not only undesir
able but also contrary to experimental findings (F. A. Miles and S. G.
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,
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VOR
Ih
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hw I
eh + 1+ "
w
----.
-{-)----
I
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:

Figure 2 Block diagram of the open-loop VOR and the negative-feedback. pursuit tracking
system. Continuous lines denote signal flow channels within the nervous system; discontinuous
lines represent exteral. physical links denoting head velocity with respect to the world
(hw). eye velocity with repect to the head (e0. eye velocity with respect to the world (ew gaze
velocity). and target veloity with respct to the world (tw).
Lisberger. in preparation). In the short term, the gain of the monkey'S VOR
seems to be fxed and immutable: No matter what the ongoing tracking
behavior or the manner in which it is being achieved. the VOR is always
active.
In sum. the VOR functions always to protect the preexisting gaze velocity
-whether zero or otherwise-thereby stabilizing whatever retinal images
are of primary interest at the time the head is disturbed. Only animals with
a pursuit system have an interest in stabilizing the retinal images of moving
targets. The rabbit, for example, does not seem able to track small targets
moving across a featured background and is, therefore, thought to lack a
pursuit system. Clearly, visual feedback in this animal always operates to
stabilize the retinal image of the stationary surroundings and, hence, the
preexisting gaze velocity that its VOR functions to protect is always zero.
Long-Term Regulation: Adaptive Gain Control
If for any reason the gain of the VOR deviates appreciably from unity,
ocular stability will be lost during head turs and persistent retinal image
slip will result. As already pointed out, because of their long latency, visual
feedback mechanisms could ameliorate but never totally eradicate this ocu
lar instability-particularly during fast head movements. Clearly, vision
would be severely compromised during head movements. Even assuming
that the genetic specifications for the VOR were exactly appropriate, it is
surely inconceivable that the refl ex could remain calibrated over a whole
lifetime. If the VOR did not possess a built-in adaptive capability, it would
be unacceptably vulnerable to minor diseases, traumas, and aging.
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LONG-TERM SENSITIVITY OF VOR TO ALTERED VISUAL INPUT It is
important to realize that the retinal events during head turs provide the
system's only truly reliable way of determining not only that a VOR calibra
tion problem exists but also the exact nature of the problem, i.e. whether
the gain is too high or too low. Persistent retinal image slip clearly signals
the need for a VOR gain adjustment. If the gain were too low (compensa
tory eye movements fail to fully ofset head rotations) then the image of the
stationary surroundings would consistently slip in a direction contrary to
the head movement, whereas the reverse would be experienced if the gain
were too high. The simplest direct test of the system's adaptive gain control
capability would be to use optical means to induce such retinal events
during head turs and then measure their efects on the gain of the VOR.
This has been achieved using magnifying or reducing telescopic spectacles
(Miles & Fuller 1974, Gauthier & Robinson 1975, Miles & Eighmy 1980).
If an animal wearing, say, 2 X magnifying telescopic spectacles keeps its
head perfectly still, no new demands are placed upon its oculomotor system.
A target that appears through the spectacles to be 10 of to one side can
be foveated with a 10 saccadic eye movement (although in reality the target
is only 5 of to one side); likewise, a target seen moving across the feld of
view at 10 per sec can be tracked with a matching eye velocity of 10 per
sec (although in reality the target is only moving at 5 per sec). Only if the
animal moves its head will it face a new challenge: if the head rotates at,
say, 10 per sec, the world seen through the spectacles will move at twice
that rate. Thus, in order to keep the images on its retina stable during head
turs, the animal would have to double the usual velocity of its compensa
tory eye movements.
With 2 X magnifying telescopic spectacles, the gain of the monkey'S VOR
(measured in the dark) shows a gradual increase that is roughly exponential
and achieves an asymptote about 1.7 times normal in a few days. Con
versely, 0.5 X reducing spectacles bring about a gradual reduction in the
gain ofthe VOR to about 0.7 times normal (Miles & Eighmy 1980). Because
these changes always operate to improve stability of the retinal image
during head turs, the system is said to possess adaptive gain control.
It should be appreciated that in order to disturb the visual input asso
ciated with head movements in a way that will challenge the adaptive
capability of the VOR, the optical device must move with the head and not
with the eyes. Magnifying contact lenses (even assuming such an optical
arrangement is possible) that move with the eyes would call for a change
in the "gain" of the system that translates retinal image eccentricity into
a rapid saccadic eye movement, but would not present a new challenge to
the VOR: retinal image stability during head tums would still require a
VOR gain of unity.
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A variety of optical means have been employed in a variety of diferent
animal species to demonstrate adaptability in the VOR; all have in common
the characteristic of disrupting the visual input associated with head move
ments and all result in gradual, adaptive changes in the gain of the re
fex.1 However, it is clear that gain is not the only regulated parameter in
the VOR. For example, optical-reversal of vision can elicit highly complex
adaptions that afect phase as well as gain (Gonshor & Melvill Jones
1976b, Melvill Jones & Davies 1976, Miles & Eighmy 1980); our under
standing of the mechanisms operating in such situations is at present rudi
mentary.
THE SYSTEM HAS MEMORY Once an appropriate VOR gain has been
achieved, it would clearly be advantageous for the system to retain the gain
without needing continual recalibration. A system that is modifiable and
has the ability to retain the modified state without reinforcement is said to
be plastic. That the VOR has "memory" and undergoes changes of a
long-term nature is evident from its ability to endure prolonged periods
(days) without any "visual reinforcement," e.
g
. total darkness or head
immobilization (Robinson 1976, Miles & Fuller 1974, Miles & Eighmy
1980). The VOR is particularly stable in its normal or low-gain state and
shows no significant gain changes during head immobilization at least for
periods up to one week. The high-gain state is somewhat more labile,
showing some very gradual recovery back toward a more normal gain
(unity) in the absence of coordinated visual-vestibular experience; however,
some consolidation process seems to be involved here since the recovery
becomes less severe and less rapid following longer exposures to the magni
fying spectacles.
CHANGES ARE "SEMI-PERMANENT" AND NOT SIMPLY A LEARNED
STRATEGY In the absence of any biophysical or morphological evidence
we can only speculate about the mechanisms subserving this adaptive capa
bility of the reflex. However, the long-term nature of the adaptive gain
changes in the VOR encourages us to believe that this system contains
"modifiable synapses" and that it will eventually yield insights into some
of the cellular mechanisms underlying memory and learing. In this regard,
it is particularly important to try to establish that the adaptive changes are
'Species include humans (Gonshor & Melvill Jones 1971, 1976a, 1976b, Gauthier & Robin
son 1975), monkeys (Mile & Fuller 1974, Miles & Eighmy 1980), cats (Robinson 1976, Melvill
Jones & Davies 1976, Keller & Preht 1979), rabbits (Collewijn & Grootendorst 1978, 1979,
Ito et al 1974, Ito et al 1979a), birds (Green & Wallman 1978) and fsh (Schairer & Bennett
1977, 1978).
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due to genuine "modifications" in the basic reflex and are not due to some
immediate parametric adjustment resulting only from some leared strat
egy. Such "behavioral" influences clearly would not involve any synaptic
modifications in the refex.
In the monkey, there are several pieces of evidence to suggest that the
adaptive gain changes associated with telescopic spectacle experience refect
"semi-permanent" changes in the fundamental refex (Miles & Eighmy
1980):
1. Neither the rate of adaptation to telescopic spectacles nor the rate of
recovery following their removal speeds up with repeated exposures, as
might have been expected if the animals had merely been leaing some
strategy that could be used at any time to adjust the magnitude of their
compenstory eye movements. Indeed, the changes in gain usually pro
ceed in an almost machine-like way, the rate being very similar even in
diferent individuals.
2. Standard caloric tets of vestibulo-ocular function in the adapted ani
mals reveal changes in responsiveness that closely parallel the gain
changes seen with the usual passive oscillation tests. Given the vastly
diferent contextual information available to the animal in these two test
situations, one might have expected very diferent results if strategy
specifc parametric adjustments had been involved.
3. In the head immobilization experments mentioned earlier to test for
retention, several days may have elapsed since the animal last wore the
adapting spectacles, yet its VOR gain still retains the adapted state. It
seems doubtful that the animal would continue to employ a strategy for
which there is no longer any apparent, continuing need.
4. The magnitude of the short-latency compensatory eye movements gener
ated by the VOR in response to sudden, unexpected disturbances of the
head is simply a function of the measured gain of the refex. Even an
elevated VOR gain (following adaptation to magnifying spectacles) is
unafected in situations where zero gain might seem preferable, e.g. in
tracking a target that moves with the head, requiring that the animal
attempt to keep its eyes stationary in its moving head (S. G. Lisberger
and F. A. Miles, in preparation). Thus, i the short term, the gain of the
VOR is fixed and immutable.
Unfortunately, such tests have not yet been carried out in any species
other than monkey and the situation in man, in particular, is far from clear.
The magnitude of the compensatory eye movements generated by human
subjects in the usual VOR test situation is known to depend upon the
instructions given to them (Barr et al 1976). Whatever mechanism is at
work here makes it difcult to estimate the gain ofthe "basic" reflex in man,
and renders the interpretation of human adaptation data problematical.
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A STORED PATTERN? It has been suggested that in the rabbit, VOR
adaptation involves the formation of memory traces representing specific
motor patters that can be emitted when the requisite stimulus conditions
recur (Collewijn & Grootendorst 1979). This suggestion arose in part from
the fnding that adaptation elicited by passive sinusoidal oscillation of the
head was relatively specific for the oscillation frequency used and that very
occasionally the eyes continued to oscillate at that same frequency even
when the animal was stationary in total darkness (Collewijn & Grooten
dorst 1979). Although the frequency-specificity of adaptation is also appar
ent in rhesus monkey (Miles & Lisberger 1980), we have ofen looked for
-but never observed-spontaneous oscillations of the eyes following adap
tation with passive oscillation in this species (F. A. Miles and S. G. Lis
berger, unpublished observations, 1980). This is only one of several
apparent diferences between the adaptive gain control processes in the
monkey and the rabbit, and others will be touched upon later.
ADAPTIVE GAIN CONTROL AS A NORMAL, EVERYDAY FUNCTION
There is reason to believe that the adaptive gain changes are achieved
through the extrapolation of normal physiological processes and do not
represent pathology. In the normal monkey, gain and phase of the VOR are
relatively insensitive to changes in stimulus amplitude and frequency (at
least over the range of 0. 1 to 1.0 Hz); because this continues to be true
following adaptation to telescopic spectacles, it seems that the dynamic
characteristics of the adapted reflex are relatively normal, which reinforces
the idea that we are dealing with pure gain changes and minimal side efects
(Miles & Eighmy 1980). In fact, it seems reasonable to assume that the
challenge of telescopic spectacles is met by built-in adaptive mechanisms
whose normal, everyday function is the long-term regulation of ocular
stability: we are not dealing with a laboratory curiosity. It is also clear that
the adaptive capability is not just a feature of the developing nervous system
and may even be retained throughout life (Gonshor & Melvill Jones 1976b).
SITE OF THE MODIFIABLE ELEMENTS IN THE
VOR
If the adaptive gain control mechanism in the VOR is to contrbute to our
understanding of the cellular mechanisms underlying motor leaing in the
central nervous system, there is a most urgent need to locate the site of its
modifiable elements. Largely as a result of the work and the writings of Ito
(1970, 1972, 1974, 1977) interest has centered initially on the vestibular part
of the cerebellum.
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PLASTICITY IN VESTIBULa-OCULAR REFLEX 283
The Cerebelar Hypothesis
Ito applied the rather general Marr-Albus cerebellar model of motor lear
ing (Marr 19 69, Albus 1971) to the specific case of the VOR. Based on his
knowledge of the anatomical arrangements in this system in the rabbit, Ito
developed the idea of the vestibular cerebellum-r more particularly, the
focculus-as a side-loop of the VOR that might act as the variable gain
element in the system. Thus, he envisaged that the cerebellar cortical net
works, carrying vestibular signals originating from mossy-fiber inputs,
would contain modifiable synapses whose efcacy was under climbing-fiber
control. Furthermore, he recognized the utility of the retinal image slip
associated with each head tur as a potential error signal that the system
might use to guide adaptation, and he suggested that the climbing fibers
might, therefore, transmit visual information. The subsequent finding that,
in the rabbit at least, the climbing fbers not only received visual inputs
(Maekawa & Simpson 1973) but were directionally selective (Simpson &
Alley 1974), was nicely consistent with the hypothesis. However, the major
evidence that sustained the plausibility of this hypothesis was the efect of
cerebellar leions: in all of the species examined, lesions of the cerebellum
that included the vestibular portion resulted in a loss or severe defcit in
adaptive gain control in the VOR (Ito et al 1974, Robinson 1976, Schairer
& Bennett 1980, Optican et al 1980). However, recent single unit studies in
the monkey focculus argue strongly against this hypothesis in this species
and suggest alterative explanations for the lesion deficits.
THE PRIMATE FLOCCULUS: NORMAL PHYSIOLOGY In order to re
view this recent evidence satisfactorily it is frst necessary to establish the
normal physiological role of the focculus. In the monkey, the focculus is
much more than a side-loop of the VOR. Single unit studies of the activity
that originates from mossy-fiber inputs (Lisberger & Fuchs 1978, Miles et
al 1980b), reveal that, in addition to carrying vestibular signals encoding
angular head velocity (measured with respect to the surroundings), its
Purkinje output cells (P-cells) also discharge in relation to eye velocity
(measured with respect to the head). In fact, these two components of P-cell
discharge are, on the average, of similar strength, have the same directional
preference, and sum algebraically to efectively encode gaze velocity (move
ment of the eyes with respect to the surroundings).
Since the monkey's VOR gain is normally close to unity, its gaze velocity
during head turs is close to zero and the P-cells in the focculus show little
if any modulation of their discharge. Thus, these P-cells normally make
little or no contribution to the VOR. In fact, appreciable modulation of the
activity of these cells is evident only when the animal tracks moving targets;
furthermore, being related to gaze velocity, this modulation is relatively
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independent of whatever combination of eye and head movements the
monkey opts to use. Lesions of the primate focculus result in large defcits
in pursuit that are roughly equally severe whether the animal attempts to
employ movements of its eyes alone or in combination with head move
ments (Zee et al 1978); this is consistent with the idea that these P-cells
normally function to boost the performance of the smooth tracking system
by contributing a gaze velocity signal.
In Figure 3 we have incorporated these gaze-velocity P-cells into the
signal fow model of the VOR and pursuit system presented earlier. The
head velocity component of P-cell discharge seems to be vestibular in origin
and is confgured in the model as part of an inhibitory side-loop of the
vestibulo-ocular pathway, whereas the eye velocity component is assumed
to be related to the motor command to move the eyes (though it may result
from aferent input) and is configured as part of a positive-feedback loop.
The existence of the latter has long been predicted by theoreticians intent
upon modeling the pursuit system (Fender & Nye 1961, Fender 1962,
Young et al 1968, Robinson 1971), and positive-feedback is commonly
employed by engineers to boost the gain of negative-feedback control sys
tems. However, as discussed earlier, monkeys ofen accomplish pursuit
tasks with combined eye-head movements, substituting part of the eye
movement with a head movement. It is in this situation, where the ocular
component of pursuit (and hence the eye-velocity, positive-feedback boost
through the flocculus) is diminished, that the vestibular (head velocity)
component of P-cell discharge plays a crucial role in the process: it makes
up for the drop in the eye velocity component. This ensures that the output
from the focculus continues to provide the same gaze velocity signal in
support of tracking whether the head is stationary or moving. It will also
be apparent from Figure 3 that the vestibular component of P-cell discharge
efectively operates to counter-balance the brainstem vestibular drive gener
ated by the head component of the tracking gesture.
In summary, the primate flocculus does not normally contribute signif
cantly to the gain of the VOR but is concered rather with boosting the gain
of the pursuit system; since this boost is in the form of a gaze velocity signal,
the pursuit system derives equal benefit no matter what combination of eye
and head movement the animal chooses to deploy.
THE PRIMATE FLOCCULUS: VOR ADAPTATION Although it has
become clear that the primate flocculus does not operate in the fashion
envisaged by Ito (1972) for the rabbit it might still contain the modifable
elements subserving adaptive gain control in the VOR. In the signal flow
diagram in Figure 3, it is evident that the gain of the VOR is actually
dependent upon the gains of several elements, designated A, B, C, and D
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r-----------------------------------,
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----
Eye -_;-.---
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=------~-&---~-&-
Figure 3 Block diagram of the VOR and pursuit system, incorporating the gaze velocity
P-cells in the focculus. Continuous lines denote signal flow channels within the nervous
system; discontinuous
.
lines represent exteral, physical links denoting head velocity with
respect to the world (hw). eye velocity with respect to the head (ei, eye velocity with respect
to the world (e. gaze velocity), and target velocity with respect to the world (i.). A. B. C.
and D represent gain elements; h'. and I'b denote the head velocity and eye velocity inputs.
respectively, to the P-cells in the focculus whose discharge modulations efectively encode gaze
velocity (
I
'.).
in the fgure, any one or more of which might be "modifiable." The follow
ing simple expression describes the gain of the VOR:
Gain of VOR
-C(D -A)
1- B
2.
An increase in the gain of the VOR might be achieved by increases in C,
D, or B, and/or a decrease in A. (Note that the gain of the refex has a
negative value since its output is opposed in direction to its input.)
Single unit recordings in the primate focculus (Miles et .al 1980a) have
revealed that the average strength of the head velocity (vestibular) signals
carried by the P-cells varies with the gain of the VOR. Adaptation to
magnifying spectacles, for instance, was associated with an increase in the
average gain of this component, which was very comparable in magnitude
to the increase in the gain of the VOR. In Figure 3, the strength of the
vestibular signal recorded at the P-cell depends upon the gains of elements
A and C. However, E. 2 shows that an increase in the gain of element
A in the focculus would operate to decrease the VOR gain; it would be.
necessary to invoke additional changes outside the flocculus-in element D
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-to achieve the observed increase in VOR gain. In that case, element D
would be properly regarded as the modifiable element subserving adaptive
gain control in the refex. If, on the other hand, the changes recorded at the
P-cell were due to modifcations in element C, then the focculus and the
brainstem relay would both receive a vestibular signal of changed gain;
such modications would, therefore, account for the observed increases
in the gain of both the VOR and the vestibular component of P-cell
discharge. Although the available data do not distinguish between the two
possibilities, it is nonetheless clear that the modifable elements subserv
ing VOR gain changes lie outside the focculus (elements C and/or D in
Figure 3).
It will be recalled that these P-cells normally contribute little to the VOR,
their activity being only very weakly modulated during head turs, and unit
recordings reveal that this remains true in the adapted animals, at least in
the high-gain state. The increase in the magnitude of the compensatory eye
movements coupled to head turs in the high-gain animal means that the
eye velocity input to the P-cell associated with a given head tum will be
proportionately higher than normal; however, this potential threat to the
usual balance between head- and eye-velocity signals at the P-cell is ofset
by the above-mentioned concomitant increase in the P-cells' sensitivity to
head velocity. Thus, the increased eye velocity input to the flocculus, which
is due directly to the increase in the gain of the VOR. is counter-balanced
by a proportional increase in the head velocity input. The net result is that
the P-cells continue to show little discharge modulation during head turs
in the adapted animal and hence continue to make little contribution to the
VOR.
If the observed changes in the P-cells' vestibular signals are not responsi
ble for the change in the gain of the VOR. then it is pertinent to ask what
purpose they accomplish. In fact, if such changes did not occur, the floc
culus would be less efective in carrying out its important supporting role
in combined eye-head tracking. It was pointed out above that the vestibular
component of P-cell discharge is important in counter-balancing the ves
tibular drive generated in the brainstem by the head component of the
tracking maneuver. Accordingly, any changes in the "gain" of the brain
stem vestibular signal should be matched by corresponding changes in the
"gain" of the focculus vestibular signal: the one should be regulated in
harmony with the other. In summary, the changes in the vestibular sen
sitivity of the P-cells are a secondary consequence. rather than a primary
cause. of the change in VOR gain. and these changes enable the focculus
to continue to provide appropriate support for the pursuit system during
head movements in the adapted animal.
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FLOCCULUS RECORDINGS IN OTHER SPECIES It has been reported
that the P-ceUs in the rabbit's flocculus change their discharge modulation
during oscillation in the dark in association with changes in the gain of the
VOR (Dufosse et al 1978a, Ito 1977). Unfortunately, the signal content of
the P-cells in the rabbit flocculus has not been determined, hence the
etiology of the recorded changes is uncertain. In particular, it is not known
if these P-cells are like those in the primate and carry an eye-velocity signal.
At the present time, therefore, it is not possible to ascertain the functional
significance of these fndings.
WHY DO FLOCCULUS LESIONS COMPROMISE ADAPTIVE GAIN CON
TROL? It is pertinent at this point to ask why focculus lesions, even in
the primate, eliminate adaptive gain control in the VOR so efectively if, as
we assert above, the single unit recording evidence is against the view that
the focculus of monkeys contains the modifiable elements. One possibility
is that the known deficits in the animal's pursuit system undermine its
ability to stabilize the retinal images seen through the telescopic spectacles
so severely as to efectively disrupt the adaptive mechanism. In this event,
the loss of adaptive capability is secondary to an oculomotor insufciency.
A second, and in our view more likely, explanation is that the output from
the focculus is important in the induction of the modifcations underlying
adaptive gain control in the VOR pathways, i.e. it provides all or part of
the error signal guiding recalibration of the refex (Miles et al 1 980a). We
shall retur to this point in some detail below.
Similar explanations might be advanced to explain the elimination of
adaptive gain control in the VOR by olivary lesions that destroy the climb
ing fber input to the flocculus (Ito & Miyashita 1975, Haddad et aI1980).
It has recently been shown that destruction of the climbing fbers in the
rabbit has a dramatic efect on the target P-ce1ls, which lose their customary
inhibitory action on the vestibular relay cells in the brainstem (Dufosse et
al 1978b, Ito et al 1978, 1979b). Thus, lesions of the olive may be expected
to mimic lesions of the flocculus.
The Brainstem Hypothesis
In the monkey, all of the pertinent evidence suggests that the modifiable
elements underlying gain changes in the VOR are not in the focculus (Miles
et al 1980a). This, and the fact that VOR gain changes are evident in even
the shortest-latency vestibulo-ocular responses that follow sudden distur
bances of the head (S. G. Lisberger and F. A. Miles, in preparation), focuses
new attention on the brainstem and suggests that the modifiable elements
might even be found in the direct VOR pathways having only two or three
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synapses. Furthermore, i the adaptation is specifc to the VOR, then one
might expect that in general the neural changes would occur at an early
stage in the pathway, before the points at which other signals related to the
generation of other kinds of eye movements are introduced. It would seem
potentially most disruptive for the modifiable elements to be located in those
parts of the pathway that are shared with other systems. We assume, after
all, that these other systems did not come under any adaptive pressure.
However, compelling though these arguments may seem, recent evidence
suggests that some nonvestibular oculomotor control signals are routed
through these modifiable gain elements (Lisberger et al 1980). Indeed, the
efect of VOR gain changes on various quantitative measures of oculomotor
performance has revealed some new aspects of the central organization of
the oculomotor system.
CONVERGENCE OF OCULOMOTOR CONTROL SIGNALS: "BEHAV
IORAL ANATOMY" Population studies examining the vestibular sen
sitivity of semicircular canal primary aferents and of cells in the meial
vestibular nuclei that receive inputs from these aferents have failed to
reveal any evidence for signifcant neural changes associated with four-fold
changes in the gain of the VOR (Miles & Braitman 1980, Lisberger & Miles
1980). This implies that the modifable elements must lie beyond the frst
central synapse in the VOR pathway. However, it is generally assumed that
the optokinetic and vestibulo-ocular pathways converge at the level of the
second-order neurons, and discharges related to optokinetic stimulation
have been extensively documented in the very cells of the medial vestibular
nuclei that were unafected by VOR adaptation (Waespe & Henn 1977). It
follows that the signals responsible for all or part of the optokinetic response
should share the modiable element, and that changes in VOR gain should
be accompanied by parallel changes in the gain of the optokinetic responses.
A complication here is that, as already mentioned in an earlier section,
the primate has two visual stabilization mechanisms: the pursuit and op
tokinetic systems. Both are thought to be operative in the usual optokinetic
test situation, when it is customary to record the eye movements elicited by
a continuously-moving visual field, achieved by surrounding the animal
with a rotating, striped cylinder. The resulting optokinetic nystagmus con
sists of smooth, tracking eye movements in the direction of the seen move
ment, interrupted at intervals by fast, resetting saccades in the opposite
direction. Smooth eye velocity shows an initial rapid rise that lasts for a few
hundred milliseconds, followed by a much more gradual increase that may
take 10 to 15 sec to reach asymptote (Cohen et a11977, Raphan et aI1979).
It is thought that the rapid changes are due mainly to the pursuit system,
whereas the subsequent slow changes are due to build-up in a velocity
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PLASTICITY IN VESTIBULa-OCULAR REFLEX 28 9
storage mechanism that represents the optokinetic system proper (Zee et al
1 976, Lisberger et aI1 980). If the lights are extinguished after this build-up
has commenced, then the nystagmus persists as optokinetic aftemystagmus
(OKAN), the initial intensity of which is assumed to be a direct index of
the "optokinetic" component of the prior response (Raphan et al 1 979,
Lisberger et al 1 980).
Changes in the gain of the VOR have been shown to result in dramatic
and almost proportional changes in the intensity of the slow "optokinetic"
component as indicated by the initial OKAN velocity, but not in the fast
"pursuit" response (Lisberger et al 1 980). That the changes in the "optoki
netic" component so nearly mirrored those in the gain of the VOR is
consistent with the view that they are a secondary consequence of the latter
and that the modifiable elements are for the most part located in the later
stages of the vestibular pathway that are shared with the optokinetic system.
The failure to see cbanges in the "pursuit" component of the optokinetic
response suggests that the signals driving it do not access the final oculomo
tor pathways through the modifiable elements.
These new data have been incorporated into our signal fow diagram in
Figure 4. In keeping with the arguments made in the previous section, the
putative modifable elements are located at C and D in the brainstem. The
optokinetic signal must converge on the vestibulo-ocular pathway above the
level of these elements and the pursuit signals at some later stage. However,
since focculus lesions have a devastating efect upon the gain of pursuit (Zee
et a11 978) and the "pursuit" component of the optokinetic response (Opti
can et al 1 980), these eye movements must be mediated by inputs that
converge upon the VOR pathways before the eye velocity signal is fed back
to the focculus.
OTHER SPECIES Data from other species present a somewhat diferent
picture. Keller & Precht (1 979) have reported significant changes in the
vestibular sensitivity of cells in the cat medial vestibular nuclei in associa
tion with changes in the gain of the refex. At present it is not clear if this
apparent diference between cat and monkey refects a genuine species
diference or some methodological inconsistency. Furthermore, although
changes have been reported in the optokinetic responses of the rabbit in
association with adaptive changes in the gain of the VOR (Collewijn &
Kleinschmidt 1 975, Collewijn & Grootendorst 1 979), they appear to have
a very diferent etiology from those in the monkey. Whereas the changes
in the primate optokinetic responses were viewed merely as a secondary
consequence of the variable gain element being in the later, shared portion
of the optokinetic and vestibular pathways, the changes in the rabbit's
optokinetic responses were viewed as independent of the gain changes in the
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r----------------------------------------,
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Figure 4 Block diagram of the VOR together with the "pursuit" and "optokinetic" visual
feback systems. Continuous lnes denote signal flow channels within the nervous system;
discontinuous lines repreent external, physical links denoting head veloity with repect to
the world (h,), eye veloity with repet to the head (eJ, eye velocity with repet to the world
(i. gaze velocity), target veloity with repect to the world (i.), and veloity of the visual
suround with repet to the world (s.).
vestibular system. Thus, in the rabbit, regardless of whether the gain of the
VOR increased or decreased, the optokinetic system always showed a sig
nifcant increase in gain. Since the optokinetic system is a negative-feedback
mehanism, such increases in gain would always operate to improve the
system's performance and hence could be regarded as "adaptive." It is
difcult to generate a convincing telelogical argument to justify the need
for such "adaptive improvements," since it is not clear why such a system
would not be calibrated optimally (i.e. maximally) at the outset of the
experiment. However, before accepting these data as yet further documen
tation of species diferences, it should be noted that, in the primate studies,
optokinetic responses were assessed using prolonged unidirectional stimula
tion, whereas in the rabbit studies, sinusoidal stimuli were used. A further
complication is that when occasionally both testing techniques (prolonged
unidirectional and sinusoidal) were used in the rabbit studies, they gave
contrary answers (Collewijn & Grootendorst 1979).
NATURE OF THE VOR GAIN ERROR SIGNAL
Accurate calibration of the VOR requires reliable "error" information
about its performance. As already pointed out, any shortcomings in the gain
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of the VOR will result in persistent retinal slip during head turs. Of course,
the system cannot diagnose gain errors from retinal slip alone and must
relate it in some way to the ongoing head movement. The directional
relationship between the slip and the head movement reliably indicates the
direction in which the VOR gain needs to change to achieve better image
stabilization, and most models of the adaptive mechanism derive their error
information from a comparison of visual and vestibular inputs (Ito 1 972,
Robinson 197 6, Gonshor & Melvill Jones 1 976b). The ultimate dependency
on visual and vestibular inputs is clearly obligate since they alone provide
information to the central nervous system that relates directly to the exter
nal reference- the surrounding world. However, this need not mean that
the system necessarily uses visual and vestibular inputs per se to guide
calibration: any reliable central correlates of the same might serve equally
well.
Substitutes for Vestibular (Head Velocity) Signals?
In an animal like the rabbit that never tracks moving objects, smooth eye
velocities are used solely to compensate for head movements and operate
always to stabilize the eyes with respect to the stationary surroundings. In
such a system, eye velocity signals could substitute for head velocity (ves
tibular) signals to achieve adaptive VOR gain changes: When the retinal slip
is in the same direction as the eye movement, it would indicate that the eye
velocity was not large enough, a situation that could be remedied by increas
ing the gain of the VOR; conversely, if slip and eye velocity are in opposing
directions, it would indicate the need for a decrease in the gain of the VOR.
There is evidence that, indeed, this is the modus operandi in the rabbit. i.e.
the regulated variable is an eye velocity signal rather than a head velocity
signal. With optical situations calling merely for an increase or decrease in
th gain ofthe VOR (e.g. magnifying or reducing telescopic spectacles), this
mechanism would operate appropriately and be indistinguishable from one
deriving error information from retinal slip and head velocity signals. How
ever, optical situations producing left-right mirror reversal of the visual
input have proved to be most revealing. When the rabbit was passively
oscillated, COllewijn & Grootendorst (1 979) observed that for the frst hour
or so the gain of the VOR decreased but, thereafer, showed a gradual and
consistent increase. Upon examiniRg the original eye movement records,
they observed that for the first hour or so the animal's compensatory eye
movements in the light were attenuated and normally directed but, thereaf
ter, showed reversal. Thus, although the directional relationship between
retinal slip and head movement remained unchanged throughout. the direc
tional relationship between retinal slip and eye movement underwent a
reversal that coincided with the reversal in the direction of the VOR gain
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change. When slip and eye movements were in opposing directions, the
VOR gain decreased; when the two were in the same direction, it increased.
Further evidence that the velocity of the eyes rather than of the head was
the relevant parameter was the demonstration that the gain of the rabbit's
VOR could be increaed merely by prolonged exposure to sinusoidal optoki
netic stimulation with the head fixed i position, i.e. head movements are
not even necessary (Collewijn & Grootendorst 1979).
Prolonged optokinetic stimulation is also known to increase the gain of
the VOR in fish (Schairer & Bennett 1978) but is inefective in the monkey
(Miles & Lisberger 1980). Furthermore, passive oscillation of the monkey
in left-right reversing prisms results in a decrease in VOR gain even though
the compensatory eye movements show consistent "reversal" in the light
(Miles & Eighmy 1980). Thus, the adaptive mechanism in the monkey
responds to the reversed-vision situation in the same way that it responds
to reducing spectacles; that both optical situations share the same kind of
relationship insofar as slip and head velocity are concered, while difering
in regard to slip and eye velocity, indicates once more that eye movements
per se are irrelevant. In the monkey, therefore, all of the available evidence
is consistent with the view that the system uses some direct measure of head
velocity to deduce the errors in the gain.
Substitutes for Retinal Slip Signals?
Despite our contention that the focculus is probably not the site of the
modifications underlying changes in VOR gain, lesion data belie the conclu
sion that the primate focculus has no role in adaptation. Indeed, lesions of
the focculus have a far more pronounced efect on the adaptive capability
of the primate VOR (Optican et al 1 980) than was reported in the original
studies in the cat that are so widely cited in favor of the cerebellar hypothe
sis (Robinson 1976). This leads to the proposition that the primate focculus
might play an inductive role in producing changes in VOR gain. At this
point it becomes necessary to ask whether the adaptive gain control mecha
nism uses retinal slip signals per se to guide recalibration or substitutes some
reliable central correlate. In particular, could a gaze velocity signal such as
that encoded by the P-cells in the primate focculus provide such a correlate
and so function to regulate VOR gain?
When suddenly confronted with, say, magnifying telescopic spectacles,
the normal monkey must at frst use its pursuit system during head turs
to supplement its now inadequate VOR in the attempt to stabilize the
shifting images seen through the spectacles. Thus, the challenge of tele
scopic spectacles is initially met by the pursuit system, an important part
of which is the gaze velocity signal contributed by the focculus P-cells (Zee
et a1 1978, Lisberger & Fuchs 1978, Miles et aI 1 980b). So long as the VOR
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gain is inappropriate for the new visual conditions, retinal slip will persist
during head turs and with it reliance upon the pursuit system and the
modulation of the focculus P-cells' discharge. Indeed, the extent to which
pursuit is consistently used during head turs is itself an index of the
"error" in the VOR, and the associated discharge modulation of the gaze
velocity P-ce1ls might be used by the adaptive mechanism as a substitute
for frank visual signals.
An underlying assumption here is that so long as the animal must employ
pursuit during head turs, then its VOR gain must be in need of adjustment.
In some as yet undefined way, the resultant modulation of P-cell discharge,
if persistent and associated with vestibular stimulation, is assumed to induce
appropriate changes in the modifiable gain element. It will be recalled that
the discharges of the gaze-velocity P-cells modulate consistently during
head turs only when the VOR is inappropriate for the visual conditions
and cease when adaptation is complete (Miles et al 1980a). Such behavior
is entirely consistent with the view that these cells signal VOR gain error.
The idea that the modulation of gaze velocity P-cell discharge during
head movements may be sufcient to induce VOR gain changes receives
some indirect support from recent experiments involving only foveal pursuit
targets (Miles & Lisberger 1980). Water-deprived monkeys were reinforced
with fuids for fixating a small dim target presented against otherwise totally
dark surroundings. Matters were arranged so that during the periods of
fixation, the monkey and the target were moved either in-phase or 1 800 out
of phase to mimic the gaze velocity events, and presumably also the P-cell
discharge modulation, normally associated with wearing magnifying or
reducing telescopic spectacles. This resulted in "adaptive" changes in the
gain of the VOR equal to a much a 50% of the changes produced by an
equivalent amount of experience with telescopic spectacles. These fndings
are consistent with-though hardly a pure test of-the hypothesis that the
error signal guiding recalibration of the VOR is in part the modulation of
gaze-velocity P-cell discharge; it is certainly clear, however, that apprecia
ble gain changes can be observed in the absence of peripheral retinal slip.
Nonetheless, some infuence of visual inputs clearly seems to be indicated
and the "error" in the VOR would seem to be a combination of retinal slip
and gaze velocity signals. In fact, it is possible that the focculus P-cells
provide both signals, especially since there is evidence that some of these
cells discharge in relation to motion ofthe visual surround (Noda & Suzuki
1978, Warabi et al 1979); this would also help to explain the extreme
severity of the deficits in adaptation following focculus lesions; All of the
available evidence concering the role of the focculus in the adaptive
control of the primate VOR, including single unit recordings, lesion data,
and even the above-mentioned long-term efects of pursuit on the refex, are
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consistent with the notion that the focculus provides the error signal that
regulates the gain.
Adaptive Gain Control in the Primate VOR: A New
Hypothesis
We have proposed that the modifable elements mediating adaptive gain
control in the primate VOR are (a) located in the brainstem pathway and
(b) regulated by error signals generated at least in part by the focculus
P-cells. It remains to link these two ideas into a plausible single hypothesis.
In our scheme (Figure 5), the gaze-velocity P-cells have been assigned
two quite separate functions with but one purpose: to improve the stability
ofthe retinal image. As a part of the pursuit system, their discharge modula
tion has an immediate infuence upon their target neurons through conven
tional (inhibitory) synaptic mechanisms. As a part of the system regulating
VOR gain, their persistent discharge modulation during head turs indi
cates errors in the VOR and has a long-term infuence on the efcacy of
synaptic transmission in the vestibulo-ocular pathway.
A important feature of our hypothesis is that the P-cells exert their two
diferent infuences at two diferent points in the vestibular pathway. Since
the gain of the pursuit system is very sensitive to lesions of the focculus but
not to VOR gain changes, we assume that the P-cells' short-term synaptic
action in support of pursuit is exerted down-stream of their long-term
modulatory action. In fact, in our scheme, the P-cells' long-term infuence
must be exerted above the point from which the P-cells derive their own
vestibular input. This is assumed to be at C in Figure 5, though parallel
changes at A and D. which would be operationally equivalent, albeit more
complex, cannot be ruled out. It is vital for the functioning of our model
that there be reciprocal connections between the P-cells and the vestibular
relay cells in the brainstem, and that they be organized in essence as an
interal negative-feedback loop that is concered with long-term regulation
rather than with short-term compensation. Thus, we envisage a local feed
back loop operating (very slowly) to achieve zero modulation of P-cell
discharge during head turs: persistent modulations of P-cell discharge
("errors") induce changes in the gain of the vestibular input that in tum
operate to reduce those modulations. The single unit data show that the
output of the P-cells is indeed regulated in this manner and produces
minimal discharge modulation during head turs in the fully adapted state.
The problem now is to explain how a control loop that is entirely interal
and functions to regulate P-cell discharge can at the same time efectively
achieve an appropriate VOR gain.
In the example that follows it will be seen that the crucial factor is the
eye-velocity input to the P-cell: this signal is assumed to retain a reliable,
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PLASTICITY IN VESTIBULO-OCULAR REFLEX 2 9 5
r - - - - - - - - - - -- ---- - --- - - ------ - - - - - - - ,
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Figure 5 Block diagram of the VOR and the pursuit system, indicating the hypothesized
long-term, regulatory infuence of the gaze-veloity P-cells (broad stipple arrow) on the
postulated modifiable gain elements in the vestibular pathway (element C). Continuous lines
denote signal fow channels within the nervous system; discontinuous lines represent exteral,
physical Jinks denoting head velocity with respect to the world (h w), eye velocity with respect
to the head (eJ, eye velocity with repect to the world (ew, gaze velocity), and target velocity
with repect to the world (iw)'
constant relationship to eye velocity (something that could be achieved by
an interal negative-feedback network within the cerebellar cortex) and to
provide the interal standard against which everything else must be cali
brated.
Consider the chain of events set in motion when the nonal monkey first
wears magnifying, telescopic spectacles. Initially, there is considerable reti
nal slip during head turs and the pursuit system takes on the immediate
responsibility of augmenting the compensatory eye movements generated
by the now-inadequate VOR. In the focculus, this registers as an elevated
eye velocity signal input to the P-cell, whose discharge as a consequence
now modulates during head turs. In efect, this eye velocity signal is the
P-cells' external reference and, together with any visual inputs that they
may also receive (not indicated in Figure 5), it provides the P-cells' only link
(albeit indirect, via the pursuit system) with the exteral visual world. If the
monkey continues to wear the spectacles, the persistent modulation of P-cell
discharge due to the elevated eye velocity signal input is assumed to induce
a gradual increase in the gain of element C. This would result in (a) an
increase in the gain of the VOR, which would gradually transfer the burden
of generating larger compensatory eye movements from the pursuit system
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2 9 6 MILES & LISBERGER
to the VOR, and (b) an increase in the head velocity signal input to the
flocculus P-cells, which would operate to ofset the augmented eye velocity
signal and, hence, gradually reduce the P-cells' discharge modulation. We
assume that this process would continue until eventually the P-cells are
receiving head-velocity inputs that once more balance their eye velocity
inputs during head turs in the light. Note that at all times during the
adaptation, P-cell discharge modulation will be minimal during head turs
in the dark. When VOR gain becomes appropriate for the visual conditions,
head turs in the light will be associated with the same compensatory eye
velocities as head turs in the dark, and modulation of P-cell discharge will
be minimal. At this point, we have come full circle: the responsibility for
generating the now-larger compensatory eye movements has shifted from
the pursuit system back to the vestibular, and the error signal (P-cell
discharge modulation) has retured to zero.
SUMMARY
The vestibulo-ocular refex functions to prevent head movements from
disturbing retinal images by generating compensatory eye movements to
ofset the head movements. In the monkey-the species mainly under con
sideration here-this reflex is machine-like and very efective. In the short
term, the VOR operates as an open-loop control system without the benefit
of feedback and its performance is fxed and immutable: No matter what
patter of eye-head coordination the animal uses to view exteral objects,
there is a continuing need for the VOR and it continues to operate; however,
should the VOR consistently fail to stabilize the retinal images during head
turs, it will gradually undergo long-term adaptive gain changes that re
store that stability. This adaptive capability is ultimately dependent upon
vision, and a variety of optical devices that disturb the visual input normally
associated with head turs have been used to induce large changes in the
refex. Insofar as the monkey is concered, all of the available evidence
suggests to us that the modiable elements underlying these long-term
adjustments are located in the brainstem vestibular pathways and not, as
previously suggested by others, in the foccular lobes of the cerebellum.
However, the focculus does appear to have an important, inductive role in
the adaptive process, providing at least part of the error signal guiding the
long-term adjustments in the brainstem. In our view, the VOR is a particu
larly well-defned example of a plastic system and promises to be a most
useful model for studying the cellular mechanisms underlying memory and
learing in the central nervous system.
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PLASTICITY IN VESTIBULO-OCULAR REFLEX 2 97
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